Background The main constraint to the fight against container-breeding mosquito vectors of human arboviruses is the difficulty in targeting the multiplicity of larval sources, mostly represented by small man-made water containers. The aim of this work is to assess the feasibility of the “auto-dissemination” approach, already tested for Aedes aegypti, as a possible alternative to traditional, inefficient control tools, against Ae. albopictus in urban areas. The approach is based on the possibility that wild adult females, exposed to artificial resting sites contaminated with pyriproxyfen, can disseminate this juvenile hormone analogue to larval habitats, thus interfering with adult emergence. Methodology We carried out four field experiments in two areas of Rome that are typically highly infested with Ae. albopictus, i.e. the main cemetery and a small green area within a highly urbanised neighbourhood. In each area we used 10 pyriproxyfen “dissemination” stations, 10 “sentinel” sites and 10 covered, control sites. The sentinel and control sites each contained 25 Ae. albopictus larvae. These were monitored for development and adult emergence. Principal Findings When a 5% pyriproxyfen powder was used to contaminate the dissemination sites, we observed significantly higher mortality at the pupal stage in the sentinel sites (50–70%) than in the controls (<2%), showing that pyriproxyfen was transferred by mosquitoes into sentinel sites and that it had a lethal effect. Conclusions The results support the potential feasibility of the auto-dissemination approach to control Ae. albopictus in urban areas. Further studies will be carried out to optimize the method and provide an effective tool to reduce the biting nuisance caused by this aggressive species and the transmission risk of diseases such as Dengue and Chikungunya. These arboviruses pose an increasing threat in Europe as Ae. albopictus expands its range.
References
[1]
Hawley WA (1988) The biology of Aedes albopictus. Journal of the American Mosquito Control Association Supplement 1: 1. doi: 10.1002/dvdy.22113
[2]
Scholte EJ, Schaffner F (2007) 14. Waiting for the tiger: establishment and spread of the Aedes albopictus mosquito in Europe. Emerging pests and vector-borne diseases in Europe 1: 241. doi: 10.1002/dvdy.22113
[3]
Renault P, Solet J-L, Sissoko D, Balleydier E, Larrieu S, et al. (2007) A major epidemic of Chikungunya virus infection on Reunion Island, France, 2005–2006. American Journal of Tropical Medicine & Hygiene 77: 727–731. doi: 10.1002/dvdy.22113
[4]
De Lamballerie X, Leroy E, Charrel RN, Ttsetsarkin K, Higgs S, et al. (2008) Chikungunya virus adapts to tiger mosquito via evolutionary convergence: a sign of things to come. Virology Journal 5: 422X–5. doi: 10.1002/dvdy.22113
[5]
Kumar NP, Joseph R, Kamaraj T, Jambulingam P (2008) A226V mutation in virus during the 2007 Chikungunya outbreak in Kerala, India. Journal of General Virology 89: 1945–1948 doi:10.1099/vir.0.83628-0. doi: 10.1099/vir.0.83628-0
[6]
Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, et al. (2007) Infection with Chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370: 1840–1846 doi:10.1016/S0140-6736(07)61779-6. doi: 10.1016/S0140-6736(07)61779-6
[7]
Beltrame A, Angheben A, Bisoffi Z, Monteiro G, Marocco S, et al. (2007) Imported Chikungunya infection, Italy. Emerging Infectious Diseases 13: 1264. doi: 10.3201/eid1308.070161
[8]
Calzolari M, Bonilauri P, Bellini R, Caimi M, Defilippo F, et al. (2010) Arboviral survey of mosquitoes in two northern Italian regions in 2007 and 2008. Vector Borne & Zoonotic Diseseas 10: 875–884 doi:10.1089/vbz.2009.0176. doi: 10.1089/vbz.2009.0176
[9]
Calzolari M, Bonilauri P, Bellini R, Albieri A, Defilippo F, et al. (2010) Evidence of Simultaneous Circulation of West Nile and Usutu Viruses in Mosquitoes Sampled in Emilia-Romagna Region (Italy) in 2009. PLoS ONE 5: e14324 doi:10.1371/journal.pone.0014324. doi: 10.1371/journal.pone.0014324
[10]
La Ruche G, Souarès Y, Armengaud A, Peloux-Petiot F, Delaunay P, et al. (2010) First two autochthonous Dengue virus infections in metropolitan France, September 2010. Euro Surveillance 15: 19676. doi: 10.1038/sj.embor.7400757
[11]
Peng HJ, Lai HB, Zhang QL, Xu BY, Zhang H, et al. (2012) A local outbreak of Dengue caused by an imported case in Dongguan China. BMC Public Health 12: 83. doi: 10.1186/1471-2458-12-83
[12]
Valerio L, Marini F, Bongiorno G, Facchinelli L, Pombi M, et al. (2010) Host-feeding patterns of Aedes albopictus (Diptera: Culicidae) in urban and rural contexts within Rome Province, Italy. Vector-Borne & Zoonotic Diseases 10: 291–294. doi: 10.1089/vbz.2009.0007
[13]
Sabatini A, Raineri V, Trovato G, Coluzzi M (1990) others (1990) [Aedes albopictus in Italy and possible diffusion of the species into the Mediterranean area]. Parassitologia 32: 301. doi: 10.1038/sj.embor.7400757
[14]
Dalla Pozza G, Majori G (1992) First record of Aedes albopictus establishment in Italy. Journal of the American Mosquito Control Association 8: 318–320. doi: 10.1038/sj.embor.7400757
[15]
Romi R, Majori G (2008) An overview of the lesson learned in almost 20 years of fight against the “tiger” mosquito. Parassitologia 50: 117–119.
[16]
Romi R, Di Luca M, Majori G (1999) Current status of Aedes albopictus and Aedes atropalpus in Italy. Journal of the American Mosquito Control Association 15: 425–427.
[17]
Toma L, Severini F, Di Luca M, Bella A, Romi R (2003) Seasonal patterns of oviposition and egg hatching rate of Aedes albopictus in Rome. Journal of the American Mosquito Control Association 19: 19–22.
[18]
Pombi M, Costantini C, della Torre A (2003) [Aedes albopictus (Diptera: Culicidae) in Rome: experimental study of relevant control strategy parameters]. Parassitologia 45: 97–102.
[19]
Romi R, Toma L, Severini F, Luca M, Boccolini D, et al.. (2009) Guidelines for control of potential arbovirus mosquito vectors in Italy. Rapporti ISTISAN-Istituto Superiore di Sanità.
[20]
Itoh T (1994) Utilization of Blood fed Females of Aedes aegypti as a Vehicle for the Transfer of the Insect Growth Regulator, Pyriproxyfen, to Larval Habitats. Tropical Medicine 36: 243–248.
[21]
Devine GJ, Perea EZ, Killeen GF, Stancil JD, Clark SJ, et al. (2009) Using adult mosquitoes to transfer insecticides to Aedes aegypti larval habitats. Proceedings of the National Academy of Science USA 106: 11530–11534 doi:10.1073/pnas.0901369106.
[22]
Trexler JD, Apperson CS, Schal C (1998) Laboratory and field evaluations of oviposition responses of Aedes albopictus and Aedes triseriatus (Diptera: Culicidae) to oak leaf infusions. Journal of Medical Entomology 35: 967–976.
[23]
Itoh T, Kawada H, Abe A, Eshita Y, Rongsriyam Y, et al. (1994) Utilization of bloodfed females of Aedes aegypti as a vehicle for the transfer of the insect growth regulator pyriproxyfen to larval habitats. Journal of the American Mosquito Control Association 10: 344–347.
[24]
Henrick C (1995) Juvenoids. Agrochemicals from natural products 147–213.
[25]
Ali A, Nayar JK, Xue RD (1995) Comparative toxicity of selected larvicides and insect growth regulators to a Florida laboratory population of Aedes albopictus. Journal of the American Mosquito Control Association 11: 72–76.
[26]
Hirano M, Hatakoshi M, Kawada H, Takimoto Y (1998) Pyriproxyfen and other juvenile hormone analogues. Reviews in Toxicology 2: 357–394.
[27]
Iwanaga K, Kanda T (1988) The Effects of a Juvenile Hormone Active Oxime Ether Compound on the Metamorphosis and Reproduction of an Anopheline Vector, Anopheles balabacensis (Diptera: Culicidae). Applied Entomology and Zoology 23: 186–193.
[28]
Sihuincha M, Zamora-Perea E, Orellana-Rios W, Stancil JD, López-Sifuentes V, et al. (2005) Potential use of pyriproxyfen for control of Aedes aegypti (Diptera: Culicidae) in Iquitos, Perú. Journal of Medical Entomology 42: 620–630. doi: 10.1603/0022-2585(2005)042[0620:PUOPFC]2.0.CO;2
[29]
Dell Chism B, Apperson CS (2003) Horizontal transfer of the insect growth regulator pyriproxyfen to larval microcosms by gravid Aedes albopictus and Ochlerotatus triseriatus mosquitoes in the laboratory. Medical and Veterinary Entomology 17: 211–220. doi: 10.1046/j.1365-2915.2003.00433.x
[30]
Gaugler R, Suman D, Wang Y (2012) An autodissemination station for the transfer of an insect growth regulator to mosquito oviposition sites. Medical and Veterinary Entomology 26: 37–45 doi:10.1111/j.1365-2915.2011.00970.x. doi: 10.1111/j.1365-2915.2011.00970.x
[31]
Facchinelli L, Valerio L, Pombi M, Reiter P, Costantini C, et al. (2007) Development of a novel sticky trap for container-breeding mosquitoes and evaluation of its sampling properties to monitor urban populations of Aedes albopictus. Medical and Veterinary Entomology 21: 183–195 doi:10.1111/j.1365-2915.2007.00680.x. doi: 10.1111/j.1365-2915.2007.00680.x
[32]
Bagheri F, Talebi K, Hosseininaveh V (2011) Biological effects of the juvenoid pyriproxyfen on the pistachio green stink bug, Brachynema germari Kol. (Hem.: Pentatomidae). Archives ff Phytopathology and Plant Protection 44: 1273–1284 doi:10.1080/03235408.2010.493749. doi: 10.1080/03235408.2010.493749
[33]
Marini F, Caputo B, Pombi M, Tarsitani G, della Torre A (2010) Study of Aedes albopictus dispersal in Rome, Italy, using sticky traps in mark-release-recapture experiments. Medical and Veterinary Entomology 24: 361–368 doi:10.1111/j.1365-2915.2010.00898.x. doi: 10.1111/j.1365-2915.2010.00898.x
[34]
Seccacini E, Lucia A, Harburguer L, Zerba E, Licastro S, et al. (2008) Effectiveness of pyriproxyfen and diflubenzuron formulations as larvicides against Aedes aegypti. Journal of American Mosquito Control Association 24: 398–403. doi: 10.1080/03235408.2010.493749
[35]
World Health Organization (2007) Pyriproxyfen in Drinking-water: Use for Vector Control in Drinking-water Sources and Containers.
[36]
Devine GJ, Killeen JF (2010) The potential of a new larviciding method for the control of malaria vectors. Malaria Journal 9: 142. doi: 10.1186/1475-2875-9-142
[37]
Facchinelli L, Koenraadt CJM, Fanello C, Kijchalao U, Valerio L, et al. (2008) Evaluation of a Sticky Trap for Collecting Aedes (Stegomyia) Adults in a Dengue-Endemic Area in Thailand. American Journal of Tropical Medicine & Hygiene 78: 904–909.
[38]
Becnel JJ, Johnson MA (2000) Impact of Edhazardia aedis (Microsporidia: Culicosporidae) on a Seminatural Population of Aedes aegypti (Diptera: Culicidae). Biological Control 18: 39–48 doi:10.1006/bcon.1999.0805.
[39]
Scholte E-J, Knols BG, Takken W (2004) Autodissemination of the entomopathogenic fungus Metarhizium anisopliae amongst adults of the malaria vector Anopheles gambiae s.s. Malaria Journal 3: 45 doi:10.1186/1475-2875-3-45. doi: 10.1186/1475-2875-3-45
[40]
Reyes-Villanueva F, Garza-Hernandez JA, Garcia-Munguia AM, Tamez-Guerra P, Howard AF, Rodriguez-Perez MA (2011) Dissemination of Metarhizium anisopliae of low and high virulence by mating behavior in Aedes aegypti. Parasite & Vectors 4: 171 doi:10.1186/1756-3305-4-171. doi: 10.1111/j.1095-8312.1990.tb01973.x
[41]
García-Munguía AM, Garza-Hernández JA, Rebollar-Tellez EA, Rodríguez-Pérez MA, Reyes-Villanueva F (2011) Transmission of Beauveria bassiana from male to female Aedes aegypti mosquitoes. Parasite & Vectors 4: 24 doi:10.1186/1756-3305-4-24. doi: 10.1111/j.1095-8312.1990.tb01973.x
