First Record of Aedes albopictus in Sinaloa, Mexico Author(s): Jose I. Torres-Avendaño, Hipolito Castillo-Ureta, Edith H. TorresMontoya, Elizabeth Meza-Carrillo, Reyna L. Lopez-Mendoza, Maria G. Vazquez-Martinez, and Jose G Rendon-Maldonado Source: Journal of the American Mosquito Control Association, 31(2):164-166. Published By: The American Mosquito Control Association DOI: http://dx.doi.org/10.2987/14-6461R URL: http://www.bioone.org/doi/full/10.2987/14-6461R

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Journal of the American Mosquito Control Association, 31(2):164–166, 2015 Copyright E 2015 by The American Mosquito Control Association, Inc.

SCIENTIFIC NOTE FIRST RECORD OF AEDES ALBOPICTUS IN SINALOA, MEXICO ˜ O,1,6 HIPOLITO CASTILLO-URETA,2,6 EDITH H. TORRES-MONTOYA,1 JOSE I. TORRES-AVENDAN ELIZABETH MEZA-CARRILLO,1 REYNA L. LOPEZ-MENDOZA,1 MARIA G. VAZQUEZ-MARTINEZ3 4,5 AND JOSE G RENDON-MALDONADO ABSTRACT. We report here the discovery of Aedes albopictus for the first time in Sinaloa state, Mexico. The mosquito larvae were collected from small water containers in the urban area of Culiacan city, Sinaloa state. Identification of the species was done primarily by morphology, followed by confirmation with polymerase-chain-reaction–based molecular method. KEY WORDS dengue virus

Arbovirus, Aedes albopictus, second internal transcribed spacer, polymerase chain reaction,

Aedes (Stegomyia) albopictus (Skuse), which is commonly known as the Asian tiger mosquito, is, together with Ae. (Stegomyia) aegypti (L.), an important vector for dengue virus (DENV) in Southeast Asia (Reiter et al. 2006). It is also known to be a competent vector for the transmission of more than 20 arboviruses under laboratory conditions (Paupy et al. 2009). The distribution of Ae. albopictus has been globally spreading from Southeast Asia, where it originated its spread, to Europe, Africa, Middle East, Australia, the Americas (Benedict et al. 2007, Caminade et al. 2012), and even to some Pacific Islands (Guillaumot et al. 2012). The global spread of Ae. albopictus is mainly caused by anthropogenic activities, such as intercontinental trade (Paupy et al. 2009). In the Americas, Ae. albopictus was first found in 1985 in Harris County, Texas (Womack, 1993) and has since been spreading over the continents. In Mexico, Ae. albopictus was recorded first in Matamoros, Tamaulipas (Francy et al. 1990), followed by Ciudad Acun˜a and Piedras Negras (29u189N, 100u579W, elevation 300 m and 1 Laboratorio de Conservacion de la Fauna Silvestre, Unidad Academica Escuela de Biologia, Universidad Autonoma de Sinaloa, Avenida de Las Americas y Boulevard Universitarios S/N, Culiacan, Sinaloa, Mexico 80010. 2 Laboratorio de Biologia Molecular, Unidad Academica Escuela de Biologia, Universidad Autonoma de Sinaloa, Avenida de Las Americas y Boulevard Universitarios S/N, Culiacan, Sinaloa, Mexico 80010. 3 Centro Regional de Investigacion en Salud Publica, Instituto Nacional de Salud Publica, Colonia Centro, Tapachula, Chiapas, Mexico. 4 Posgrado en Ciencias Biome´dicas, Facultad de Ciencia Quimico Biologicas, Universidad Autonoma de Sinaloa, Avenida de Las Americas y Boulevard Universitarios S/N, Culiacan, Sinaloa, Mexico 80010. 5 To whom correspondence should be addressed. 6 These authors contributed equally in this work.

28u429N, 100u319W, elevation 320 m, respectively) in Coahuila (Iba´n˜ez-Bernal and Martı´nezCampos 1994) and Ciudad Allende (25u179N, 101u019W, elevation 674 m), Nuevo Leo´n (OrtaPesina et al. 2001), the northeastern state’s border with the United States, and then in Martı´nez de la Torre, Veracruz (Flisser et al. 2002) along the Gulf of Mexico. Subsequently, Ae. albopictus was found in Tapachula, Chiapas on the southeastern border to Guatemala (Casas-Martı´nez and Torres-Estrada 2003). Recently this mosquito has been found in the localities of Jocutla, Cuautla, and Vicente Guerrero, Morelos (Villegas-Trejo et al. 2010) and Cancun, Quinta Roo (Salomo´nGrajales et al. 2012) (Fig. 1). We performed mosquito faunal diversity study in an urban area at the University Campus in Culiacan, Sinaloa (24u49937.270N, 107u22948.089W, elevation 62 m), on January 2014. Ten plastic containers of around 5 liters were analyzed at random; they were outdoors next to the building of the School of Biology. All the retrieved water was filtered to recover larvae, which were washed 3 times with running water. A total of 119 mosquito larvae were collected from 3 bottles containing water, and 50 of them were identified morphologically as Ae. albopictus and 69 as Ae. aegypti. Among those, 12 larvae of Ae. albopictus and 21 of Ae. aegypti were fixed in absolute ethyl alcohol. Additionally, all residual samples were placed into plastic containers where 38 adults of Ae. albopictus (27 females and 11 males) and 48 adults of Ae. aegypti (30 females and 18 males) were successfully developed. Mosquito larvae and adults were identified according to the taxonomic keys of Darsie and Ward (2005). The morphological identification of mosquito species was confirmed further by molecular techniques. For this purpose, total DNA was obtained individually from adult specimens with the use of the Wizard SV Genomic DNA Purification System kit (Promega, Madison, WI) according to the

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Fig. 1. Geographic distribution of Aedes albopictus in Mexico. Previously recorded in Matamoros, Tamaulipas (1); Ciudad Acun˜a and Piedras Negras, Coahuila (2); Ciudad Allende, Nuevo Leo´n (3); Martı´nez de la Torre, Veracruz (4); Tapachula, Chiapas (5); Jocutla, Cuautla, and Vicente Guerrero, Morelos (6); Cancun, Quintana Roo (7); and this report from Culiacan, Sinaloa (8).

manufacturer’s recommendations. The ribosomal second internal transcribed spacer (ITS2) was amplified by polymerase chain reaction (PCR) with the use of the GoTaq Green Master Mix Kit (Promega) according to the manufacturer’s recommendations. To amplify the complete ITS2, 50 ng/ml of total DNA and 5 mM the CP-P1A (59-gtggatcctgtgaactgcaggacacatg-39) and CP-P1B (59-gtgtcgacatgcttaaatttagggggta-39) primers were

used. A negative control (H2O en lieu of DNA template) was included in each run (Wesson et al. 1992, Byrd et al. 2011). Amplification cycling conditions were 94uC for 5 min followed by 35 cycles of 94uC for 1 min, 54uC for 30 sec, and 72uC for 1 min. The PCR products were visualized on a 1.5% agarose gel. The CP-P1A/P1B primer pair produces a 600–base pair (bp) fragment for Ae. albopictus that differs from Ae. aegypti

Fig. 2. Identification of Aedes albopictus. (A) Agarose gel electrophoresis of 600 base pairs (bp) of ITS-2 polymerase-chain-reaction products of Aedes albopictus (Lane 3), and 360-bp fragment of Ae. aegypti (Lanes 2 and 4). Lane 1 is a negative control (H2O instead of DNA template). M 5 land marker 1 Kb (Promega, Madison, WI). (B) Adult male of Ae. albopictus (403). Arrow shows the white line on the thorax of the mosquito.

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(360 bp) (Fig. 2). Purification and sequencing of PCR products are currently underway in our laboratory. The DENV is the most widespread arbovirus that is endemic in over 100 countries including Mexico, where disease seems to spread from Chiapas in the border with Guatemala to the south of the United States (Narro-Robles and Gomez-Dantes 1995, Flisser et al. 2002). This infection is widely distributed in all Mexico and Ae. aegypti is the main vector. However, transmission of DENV and chikungunya virus among others arbovirus by Ae. albopictus have been also previously reported (Reiter et al. 2006). Although classic and hemorrhagic dengue infection transmitted by Ae. aegypti is highly prevalent in Sinaloa state (Garcı´a et al. 2011), this is the first report of Ae. albopictus in Sinaloa and the localized states in northwestern Mexico. Dengue-infected adult Ae. albopictus have not yet been reported in this area; further studies are needed in order to analyze not only the virus vector competence, which plays an integral role in virus transmission, but also because it seems to be a critical factor in determining the severity and impact of DENV outbreaks in Sinaloa. This work was supported by PROFAPI-UAS 2009/176, 2011/139, 2012/145) and Instituto de Apoyo a la Investigacio ´ n e Inovacio´n (INAPI), Gobierno de Sinaloa. E.H.T.M. was supported by CONACYT scholarship 103950. We thank Dr. Yukifumi Nawa for his criticism reviewing the manuscript and the use of English. We also thank Ruben Zamora for the mosquito picture. REFERENCES CITED Benedict MQ, Levine RS, Hawley WA, Lounibos LP. 2007. Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Dis 7:76–85. Byrd BD, Gymburch EE, O’Meara GF, Wesson DM. 2011. Molecular identification of Aedes bahamensis (Diptera: Culicidae). Florida Entomol 94:1057–1059. Caminade C, Medlock JM, Ducheyne E, McIntyre KM, Leach S, Baylis M, Morse AP. 2012. Suitability of European climate for the Asian tiger mosquito Aedes albopictus: recent trends and future scenarios. J R Soc Interface 9:2708–2717. Casas-Martı´nez M, Torres-Estrada J. 2003. First evidence of Aedes albopictus (Skuse) in Southern Chiapas, Mexico. Emerging Infect Dis 9:606–607. Darsie RF, Ward RA. 2005. Identification and geographical distribution of the mosquitoes of North

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America, north of Mexico. Gainesville, FL: University Press of Florida. p 222. Flisser A, Velasco-Villa A, Martı´nez-Campos C, Gonza´lez-Domı´nguez F, Brisen˜o-Garcı´a B, Garcı´aSua´rez R, Caballero-Servı´n A, Herna´ndez-Monroy I, Garcı´a-Lozano H, Gutie´rrez-Cogco L, Rodrı´guezAngeles G, Lo ´ pez-Martı´nez I, Galindo-Virgen S, Va´zquez-Campuzano R, Balandrano-Campos S, Guzma´n-Bracho C, Olivo-Dı´az A, de la Rosa J, Magos C, Escobar-Gutie´rrez A, Correa D. 2002. Infectious diseases in Mexico. A survey from 1995– 2000. Arch Med Res 33:343–350. Francy DB, Moore CG, Eliason DA. 1990. Past, present and future of Aedes albopictus in the United States. J Am Mosq Control Assoc 6:127–132. Garcı´a C, Garcı´a L, Espinosa-Carreo ´ n T, Ley C. 2011. Abundancia y distribucio ´ n de Aedes aegypti (Diptera: Culicidae), y dispersio´n del dengue en Guasave Sinaloa, Me´xico. Rev Biol Trop 59(4):1609–1619. Guillaumot L, Ofanoa R, Swillen L, Singh N, Bossin HC, Schaffner F. 2012. Distribution of Aedes albopictus (Diptera, Culicidae) in Southwestern Pacific countries, with a first report from the Kingdom of Tonga. Parasites Vectors 5:247. Iba´n˜ez-Bernal S, Martı´nez-Campos C.1994. Aedes albopictus in Me´xico. J Am Mosq Control Assoc 10:231–232. Narro-Robles J, Gomez-Dantes H. 1995. El dengue en Me´xico: un problema prioritario 104 de salud pu´blica. Salud Publica Mex 37:12–20. Orta-Pesina H, Mercado-Herna´ndez R, Valdez-Rodrı´guez MA. 2001. Aedes albopictus in Allende City, Nuevo Leo ´ n, Me´xico. J Am Mosq Control Assoc 17:260–261. Paupy C, Delatte H, Bagny L, Corbel V, Fontenille D. 2009. Aedes albopictus, an arbovirus vector: from the darkness to the light. Microbes Infect 11: 1177–1185. Reiter P, Fontenille D, Paupy C. 2006. Aedes albopictus as an epidemic vector of chikungunya virus: another emerging problem? Lancet Infect Dis 6:463–464. Salomo´n-Grajales J, Lugo-Moguel GV, Tinal-Gordillo VR, de La Cruz-Vela´zquez J, Beaty BJ, Lars-Eisen, Lozano-Fuentes S, Moore CG, Garcı´a-Rejo ´ n JE. 2012. Aedes albopictus mosquitoes, Yucata´n Penı´nsula, Me´xico. Emerging Infect Dis 18:525–527. Villegas-Trejo A, Manrique-Saide P, Che-Mendoza A, Cruz-Canto W, Gonza´les-Ferna´ndez M, Gonza´lezAcosta C, Dzul-Manzanilla F, Hero´n-Huerta, Arredondo-Jime´nez JI. 2010. First report of Aedes albopictus and other mosquito species in Morelos, Me´xico. J Am Mosq Control Assoc 26:321–323. Wesson DM, Porter CH, Collins FH. 1992. Sequence and secondary structure comparisons of ITS rDNA in mosquitoes (Diptera: Culicidae). Mol Phylogenet Evol 1:253–269. Womack ML. 1993. Distribution, abundance and bionomics of Aedes albopictus in southern Texas. J Am Mosq Control Assoc 9:367–369.

First Record of Aedes albopictus in Sinaloa, Mexico.

We report here the discovery of Aedes albopictus for the first time in Sinaloa state, Mexico. The mosquito larvae were collected from small water cont...
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