Biological Control of the Chagas Disease Vector Triatoma infestans with the Entomopathogenic Fungus Beauveria bassiana Combined with an Aggregation Cue: Field, Laboratory and Mathematical Modeling Assessment
Background Current Chagas disease vector control strategies, based on chemical insecticide spraying, are growingly threatened by the emergence of pyrethroid-resistant Triatoma infestans populations in the Gran Chaco region of South America. Methodology and findings We have already shown that the entomopathogenic fungus Beauveria bassiana has the ability to breach the insect cuticle and is effective both against pyrethroid-susceptible and pyrethroid-resistant T. infestans, in laboratory as well as field assays. It is also known that T. infestans cuticle lipids play a major role as contact aggregation pheromones. We estimated the effectiveness of pheromone-based infection boxes containing B. bassiana spores to kill indoor bugs, and its effect on the vector population dynamics. Laboratory assays were performed to estimate the effect of fungal infection on female reproductive parameters. The effect of insect exuviae as an aggregation signal in the performance of the infection boxes was estimated both in the laboratory and in the field. We developed a stage-specific matrix model of T. infestans to describe the fungal infection effects on insect population dynamics, and to analyze the performance of the biopesticide device in vector biological control. Conclusions The pheromone-containing infective box is a promising new tool against indoor populations of this Chagas disease vector, with the number of boxes per house being the main driver of the reduction of the total domestic bug population. This ecologically safe approach is the first proven alternative to chemical insecticides in the control of T. infestans. The advantageous reduction in vector population by delayed-action fungal biopesticides in a contained environment is here shown supported by mathematical modeling.
References
[1]
WHO (World Health Organization) Sustaining the drive to overcome the global impact of neglected tropical diseases: Second WHO report on neglected diseases. Geneva, Switzerland. 2013.
[2]
Schofield CJ, Dias JCP. The Southern Cone Initiative against Chagas disease. Adv Parasitol. 1999; 42: 1–27. pmid:10050271 doi: 10.1016/s0065-308x(08)60147-5
[3]
Lardeux F, Depickére S, Duchon S, Chavez T. Insecticide resistance of Triatoma infestans (Hemiptera, Reduviidae) vector of Chagas disease in Bolivia. Trop Med Int Health. 2010; 15(9): 1037–1048. doi: 10.1111/j.1365-3156.2010.02573.x. pmid:20545921
[4]
Germano MD, Picollo MI, Mougabure-Cueto GA. Microgeographical study of insecticide resistance in Triatoma infestans from Argentina. Acta Trop. 2013; 128: 561–565. doi: 10.1016/j.actatropica.2013.08.007. pmid:23962389
[5]
Gurevitz JM, Gaspe MS, Enriquez GF, Provecho YM, Kitron U, Gurtler RE. Intensified surveillance and insecticide-based control of the Chagas disease vector Triatoma infestans in the Argentinean Chaco. PLoS Negl Trop Dis. 2013; 7(4): e2158. doi: 10.1371/journal.pntd.0002158. pmid:23593525
[6]
Abad-Franch F, Diotaiuti L, Gurgel-Goncalves R, Gurtler RE. Certifying the interruption of Chagas disease transmission by native vectors: cui bono?. Mem Inst Oswaldo Cruz. 2013; 108(2): 251–254. pmid:23579810 doi: 10.1590/0074-0276108022013022
[7]
Stevens L, Rizzo DM, Lucero DE, Pizarro JC. Household model of Chagas disease vectors (Hemiptera: Reduviidae) considering domestic, peridomestic, and sylvatic vector populations. J Med Entomol. 2013; 50(4): 907–915. pmid:23926791 doi: 10.1603/me12096
[8]
Juarez MP, Pedrini N, Girotti JR, Mijailovsky SJ, Lorenzo Figueiras A. A trap for hematophagous insects, control and detection method of those insects. Argentine Patent P-080102268, pending. 2008.
[9]
Pedrini N, Mijailovsky SJ, Girotti JR, Stariolo R, Cardozo RM, Gentile A, Juarez MP. Control of pyrethroid-resistant Chagas disease vectors with entomopathogenic fungi. PLoS Negl Trop Dis. 2009; 3(5): e434. doi: 10.1371/journal.pntd.0000434. pmid:19434231
[10]
Forlani L, Pedrini N, Juárez MP. Contribution of the horizontal transmission of the entomopathogenic fungus Beauveria bassiana to the overall performance of a fungal powder formulation against Triatoma infestans. Res Rep Trop Med. 2011; 2: 135–140. doi: 10.2147/rrtm.s22961
[11]
Nakasuji F, Kiritani K. Estimating the control threshold density of the tobacco cutworm Spodoptera litura (Lepidoptera: Noctuidae) on a corn crop, Taro, by means of pheromone traps. Prot Ecol. 1978; 1: 23–32.
[12]
Critchley BR, Campion DG, McVeigh LJ, Hunter P, Hall DR, Cork A, Nesbitt BF, Marrs GJ, Jutsum A, Hosny M, Nasr EA. Control of pink bollworm, Pectinophora gossypyella (Saunders) (Lepidoptera: Gelechiidae), in Egypt by mating disruption using an aerially applied microencapsulated pheromone formulation. Bull Entomol Res. 1983; 73: 289–299. doi: 10.1017/s0007485300008877
[13]
Dent D. Insect pest management. Wallingford: CABI, Technology & Engineering; 2000. pp. 432.
[14]
Grant AJ, O′Connell RJ. The detection of carbon dioxide and its role in the orientation to hosts by hematophagous insects. In: Takken W, Knols BGF, editors. Olfaction in Vector-Host Interactions. Vol. 2. Wageningen: Wageningen Academic Publishers; 2010. pp. 91–114.
[15]
Carde RT, Gibson G. Host finding by female mosquitoes: mechanisms of orientation to host odours and other cues. In: Takken W, Knols BGF, editors. Olfaction in Vector-Host Interactions. Vol. 2. Wageningen: Wageningen Academic Publishers; 2010. pp 115–141.
[16]
Guerenstein PG, Lorenzo MG, Nú？ez JA, Lazzari CR. Baker’s yeast, an attractant for baiting traps for Chagas’ disease vectors. Experientia. 1995; 51: 834–837. pmid:7649243 doi: 10.1007/bf01922439
[17]
Turner SL, Li N, Guda T, Githure J, Cardé R, Ray A. Ultra-prolonged activation of CO2-sensing neurons disorients mosquitoes. Nature. 2011; 474: 87–91. doi: 10.1038/nature10081. pmid:21637258
[18]
Schofield CJ. The behaviour of Triatominae (Hemiptera: Reduviidae): a Review. Bull of Entomol Res. 1979; 69: 363–379. doi: 10.1017/s0007485300018897
[19]
Silva Rocha D, Jurberg J, Carcavallo RU, Cunha V, Galv？o C. Influência da temperatura e umidade na biologia de Rhodnius neglectus Lent, 1954 em laboratório (Hemiptera, Reduviidae,Triatominae). Rev Soc Bras Med Trop. 2001; 34(4): 357–363. pmid:11562729 doi: 10.1590/s0037-86822001000400008
[20]
Cecere MC, Canale, DM, Gürtler RE. Effects of refuge availability on the population dynamics of Triatoma infestans in central Argentina. J Appl Ecol. 2003; 40(4): 742–756. doi: 10.1046/j.1365-2664.2003.00825.x
[21]
Acu？a-Retamar M, Botto-Mahan C, Canals M, Correa JP, Cattan PE. Comparative population dynamics of the bug Mepraia spinolai, a sylvatic vector of Chagas’ disease, in different hosts. Med Vet Entomol. 2009; 23: 106–110. doi: 10.1111/j.1365-2915.2009.00795.x. pmid:19493191
[22]
Rodríguez D, Rabinovich JE. The effect of density on some population parameters of Rhodnius prolixus (Hemiptera: Reduviidae) under laboratory conditions. J Med Entomol. 1980; 17(2): 165–171. doi: 10.1093/jmedent/17.2.165
[23]
Gorla DE. Population dynamics and control of Triatoma infestans. Med Vet Entomol. 1992; 6: 91–97. pmid:1421494 doi: 10.1111/j.1365-2915.1992.tb00582.x
[24]
Spagnuolo AM, Shillor M, Stryker GA. A model for Chagas disease with controlled spraying. J Biol Dyn. 2010; 5: 299–317. doi: 10.1080/17513758.2010.505985
[25]
Cruz-Pacheco G, Esteva L, Vargas C. Control measures for Chagas disease. Math Biosci. 2012; 237: 49–60. doi: 10.1016/j.mbs.2012.03.005. pmid:22450034
[26]
Rabinovich JE. Chagas' Disease: Modeling transmission. In: Conway GR editors. Pest and pathogen control: strategic, tactical, and policy models. John Wiley & Sons. Vol 13 International Series on Applied Systems Analysis; 1984. pp 58–72.
[27]
Pelosse P, Kribs-Zaleta CM, Ginoux M, Rabinovich JE, Gourbière S, Menu F. Influence of vectors’ risk-spreading strategies and environmental stochasticity on the epidemiology and evolution of vector-borne diseases: The example of Chagas’ disease. PLoS One. 2013; 8(8): e70830. doi: 10.1371/journal.pone.0070830. pmid:23951018
[28]
Roma？a CA, Fargues J, Pays JF. Method of biological control of Triatominae, vectors of Chagas disease, using entomopathogenic Hyphomycetes. Preliminary study. Bull Soc Pathol Exot Filiales. 1987; 80:105–11. pmid:3111731
[29]
Lecuona RE, Edelstein JD, Berretta MF, La Rossa FR, Arcas JA. Evaluation of Beauveria bassiana (Hyphomycetes) strains as potential agents for control of Triatoma infestans (Hemiptera: Reduviidae). J Med Entomol. 2001; 38(2): 172–179. pmid:11296819 doi: 10.1603/0022-2585-38.2.172
[30]
Luz C, Rocha LFN, Nery GV, Magalh？es BP, Tigano MS. Activity of oil-formulated Beauveria bassiana against Triatoma sordida in peridomestic areas in central Brazil. Mem Inst Oswaldo Cruz. 2004; 99: 211–218. pmid:15250478 doi: 10.1590/s0074-02762004000200017
Juárez MP, Crespo R, Calderon-Fernandez G, Lecuona R, Cafferata LFR. Characterization and carbon metabolism in fungi pathogenic to Triatoma infestans, a Chagas disease vector. J Invertebr Pathol. 2000; 76: 198–207. pmid:11023748 doi: 10.1006/jipa.2000.4964
[33]
Pedrini N, Crespo R, Juárez MP. Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comp Biochem Physiol. 2007; 146C(1): 124–137. doi: 10.1016/j.cbpc.2006.08.003
[34]
Luz C, Fargues J, Roma？a C. Influence of starvation and blood meal-induced moult on the susceptibility of nymphs of Rhodnius prolixus Stal (Hem., Triatominae) to Beauveria bassiana (Bals.) Vuill. infection. J Appl Entomol. 2003; 127: 153–156. doi: 10.1046/j.1439-0418.2003.00733.x
[35]
Forlani L, Juárez MP, Lavarías S, Pedrini N. Toxicological and biochemical response of the entomopathogenic fungus Beauveria bassiana after exposure to deltamethrin. Pest Manag Sci. 2014; 70: 751–756. doi: 10.1002/ps.3583. pmid:23716386
[36]
Cocchiararo-Bastias LM, Mijailovsky SJ, Calderon-Fernández GM, Lorenzo Figueiras AN, Juárez MP. Epicuticle lipids mediate mate recognition in Triatoma infestans. J Chem Ecol. 2011; 37: 246–252. doi: 10.1007/s10886-011-9927-2. pmid:21373991
[37]
Caswell H. Matrix population models. Construction, analysis and interpretation, 2nd ed. Massachusetts: Sinauer Associates Inc, Publishers; 2001.
[38]
MathWorks, T Matlab. The MathWorks, Natick, MA; 2004.
[39]
R Development Core Team. R: a language and environment for statistical computing. Available from: , and used through RStudio, Version 0.98.953 - ？ 2009–2013 RStudio, Inc.; 2014.
[40]
Sobol IM. Global sensitivity indices for nonlinear mathematical models and their Monte Carlo estimates. Math Comp Simulation. 2001; 55: 271–280. doi: 10.1016/s0378-4754(00)00270-6
[41]
Ellner SP, Fieberg J. Using PVA for management despite uncertainty: effects of habitat, hatcheries, and harvest on salmon. Ecology. 2003; 84(6): 1359–1369. doi: 10.1890/0012-9658(2003)084[1359:upfmdu]2.0.co;2
[42]
Lorenzo Figueiras AN, Girotti JR, Mijailovsky SJ, Juárez MP. Epicuticular lipids induce aggregation in Chagas disease vectors. Parasit Vectors. 2009; 2:8.
[43]
Juárez MP, Brenner RR. The epicuticular lipids of Triatoma infestans. II. Hydrocarbon dynamics. Comp Biochem Physiol. 1985; 82 B: 793–803. doi: 10.1016/0305-0491(85)90527-9
[44]
Juárez MP, Brenner RR. Biochemistry of the evolutionary cycle of Triatoma infestans. V. Volatile fatty acid emission. Acta Physiol Latinoam. 1981; 31: 39–43. pmid:6139933
[45]
González Audino P, Alzogaray R, Vassena A, Masuh H, Fontan A, Gatti P, Martínez A, Camps F, Cork A, Zerba E. Volatile compounds secreted by Brindley’s glands of adult Triatoma infestans: identification and biological activity of previously unidentified compounds. J Vect Ecol. 2007; 32: 75–82. doi: 10.3376/1081-1710(2007)32[75:vcsbbo]2.0.co;2
[46]
Rojas de Arias A, Abad-Franch F, Acosta N, López E, González N, Zerba E, Tarelli G, Masuh H. Post-control surveillance of Triatoma infestans and Triatoma sordida with chemically-baited sticky traps. PLoS Negl Trop Dis. 2012; 6(9): e1822. doi: 10.1371/journal.pntd.0001822. pmid:23029583
[47]
Gorla DE, Schofield CJ. Population dynamics of Triatoma infestans under natural climatic conditions in the Argentine Chaco. Med Vet Entomol. 1989; 3: 179–194. pmid:2519662 doi: 10.1111/j.1365-2915.1989.tb00497.x
[48]
Dohna HZ, Cecere MC, Gürtler RE, Kitron U, Cohen JE. Re-establishment of local populations of vectors of Chagas disease after insecticide spraying. J Appl Ecol. 2007; 44: 220–227. pmid:17710182 doi: 10.1111/j.1365-2664.2006.01243.x
[49]
Dohna HZ, Cecere MC, Gürtler RE, Kitron U, Cohen JE. Spatial Re-establishment dynamics of local populations of vectors of Chagas disease. PLoS Negl Trop Dis. 2009; 3(7): e490. doi: 10.1371/journal.pntd.0000490. pmid:19636363
Lynch PA, Grimm U, Thomas MB, Read AF. Prospective malaria control using entomopathogenic fungi: comparative evaluation of impact on transmission and selection for resistance. Malaria J. 2012; 11:383. doi: 10.1186/1475-2875-11-383. pmid:23171286
[52]
Read AF, Lynch PA, Thomas MB. How to make an evolution-proof insecticide against malaria. PLoS Biology. 2009; 7:e1000058. doi: 10.1371/journal.pbio.1000058. pmid:19355786
[53]
Koella JC, Lynch PA, Thomas MB, Read AF. Towards evolution-proof malaria control with insecticides. Evol Appl. 2009; 2: 469–480. doi: 10.1111/j.1752-4571.2009.00072.x. pmid:25567892
[54]
Blanford S, Shi W, Christian R, Marden JH, Koekemoer LL, Brooke BD, Coetzee M, Read AF, Thomas MB. Lethal and pre-lethal effects of a fungal biopesticide contribute to substantial and rapid control of malaria vectors. PLoS One. 2011; 6:e23591. doi: 10.1371/journal.pone.0023591. pmid:21897846
