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Geographical distribution of the Aedes Triseriatus Group (Diptera: Culicidae) in Mexico Adelfo Sánchez-Trinidad1, Félix Ordoñez-Sánchez1, Ma. Teresa Valdes-Perezgasga1, Francisco J. Sánchez-Ramos1, Thomas J. Zavortink2, Antonio J. Cortés-Guzmán3, and Aldo I. Ortega-Morales1 Departamento de Parasitología, Universidad Autónoma Agraria Antonio Narro Unidad Laguna, Torreón, Coahuila 27084, México, [email protected] 2 Bohart Museum of Entomology, University of California, Davis, CA 95616, U.S.A. 3 Secretaría de Salud del estado de Guerrero, Chilpancingo, Guerrero, México

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Received 5 November 2013; Accepted 20 February 2014 ABSTRACT: Aedes brelandi Zavortink is reported for the first time outside of the United States, where it has been found in northern and central parts of Mexico. Ae. triseriatus (Say) is reported in northern and central Mexico and Ae. zoosophus Dyar and Knab is recorded in southern Mexico. Collection records for these species in northern, central, and southern Mexico showing the current distribution of the Aedes Triseriatus Group are included. Journal of Vector Ecology 39 (1): 134-137. 2014. Keyword Index: Aedes brelandi, Ae. triseriatus, Ae. zoosophus, geographical distribution, Mexico.

INTRODUCTION The North American Aedes (Protomacleaya) Triseriatus Group includes four species of mosquitoes, Ae. brelandi Zavortink, 1972, Ae. hendersoni Cockerell, 1918, Ae. triseriatus (Say, 1823), and Ae. zoosophus Dyar and Knab, 1918 (Zavortink 1972, Taylor 1990). When first recognized, the group included only three species with dark tarsi, Ae. brelandi, Ae. hendersoni, and Ae. triseriatus (Zavortink 1972). Ae. zoosophus, which differs most conspicuously from these species by having broad white bands on the tarsi and was placed into the monotypic Zoosophus Group (Zavortink 1972), was added to the Triseriatus Group by Taylor (1990) after molecular and genetic studies by Munstermann et al. (1982) and Taylor (1990) showed the species to be closely related to the dark-legged species and reproductively compatible with them. Descriptions of all four species, keys to them, and distribution maps are included in the revision of Protomacleaya by Zavortink (1972), and keys to the species and distribution maps are also presented by Darsie and Ward (2005). The immature stages of species in the Triseriatus Group usually occur in water-filled cavities in trees. These are most frequently rot-cavities caused by decay of the wood following its exposure through injury to the tree, but are sometimes pans, i.e., bark-lined depressions in the branches, crotches, or exposed roots of trees that hold water. The immatures are sometimes found in rock-holes and, in environments degraded by humans, they may also be found in water-holding artificial containers such as bottles, cans, vases, and automobile tires, particularly if these are shaded and include plant debris such as fallen leaves, twigs, flowers, and fruits. Females of all species of the group are known to bite humans (Carpenter and LaCasse 1955, Zavortink 1972). The distributions of the species of the Triseriatus Group are fairly well known in the United States. Ae. triseriatus and Ae. hendersoni occur throughout the eastern states, where they are the most common treehole-breeding mosquitoes. The former species extends westward to approximately the 100th meridian, while the latter extends farther west to the eastern slope of the Rocky

Mountains and in the north, where it has breached the Continental Divide, it occurs in the Columbia-Snake River drainage system. Both these species also make minor incursions into southern Canada. Ae. zoosophus has a more restricted distribution in the south-central states from west Texas to central Kansas and eastern Arkansas. The Triseriatus Group species with the most restricted distribution in the United States is Ae. brelandi, which is known from only the Chisos Mountains in the Big Bend area of west Texas. The distributions of species in the Triseriatus Group are less well known in Mexico. Ae. triseriatus has been reported previously from several northeastern, central, and southern Mexican states (Vargas 1956, Díaz-Nájera and Vargas 1973, Ibáñez and Martínez 1994, Muñoz-Cabrera et al. 2006) and Ae. zoosophus has been reported from northeastern and tropical parts of the country (Vargas 1956, Zavortink 1972, Díaz-Nájera and Vargas 1973, Ibáñez and Martínez 1994, Aguirre et al. 2008, Ortega et al. 2013). It is possible that some of the records reported by Vargas (1956) and repeated in subsequent papers are inaccurate because they were made before the studies of Schick (1970) and Zavortink (1972) clarified the species of Protomacleaya found in Mexico. The present study updates and summarizes our knowledge of the geographical distributions of the Triseriatus Group in Mexico as determined by our collections and examination of specimens in three Mexican collections. Ae. triseriatus is the main vector of La Crosse virus (LACV), which causes a disease that affects the central nervous system and can be severe and deadly, with children 16 years old or younger constituting the most susceptible group. Since the 1990s, this disease has had a prevalence of 50 cases per year in the United States, although during 2001 and 2002, the Centers for Disease Control and Prevention reported an incidence of 170 cases. In Mexico, the official norm NOM-032-SSA2-2010 for Epidemiological Survey, Prevention and Control of Vector Transmitted Diseases proposes the epidemiological vigilance of some diseases transmitted by mosquitoes such as dengue, West Nile virus, and malaria. LACV is not currently surveyed in Mexico, so its prevalence and incidence

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Entomological collections reviewed Specimens in three Mexican entomological collections were reviewed: Insect and mite collection of medical importance (IAIM), located at the Medical Entomology Laboratory of the Universidad Autónoma de Nuevo León (UANL) in Monterrey, N.L.; Arthropods of Medical Importance Collection (CAIM), located at the Entomology Department of the Instituto de Diagnóstico y Referencia Epidemiológicos (InDRE) in Mexico, D.F.; and Mosquito Collection (CC-UL), located at the Parasitology Department of the Universidad Autónoma Agraria Antonio Narro, Unidad Laguna (UAAAN-UL) in Torreón, Coahuila. Mosquito collection We have collected mosquitoes in various regions of Mexico since 2008. Immature stages were collected from natural breeding sites such as tree holes and from artificial containers. Adult mosquitoes were collected while biting or landing on humans. These were collected using a mouth aspirator and then put into a killing jar with triethylamine as the lethal agent. They were carried to the lab to be mounted using entomological pins and placed in the Culicid collection (CC-UL) in the Parasitology Department of the UAAAN-UL. Specimens collected in the state of Querétaro were placed alive in resting chambers where they were fed with human blood and sugar water. Later, humidified cotton was provided for the females to oviposit in the hopes of obtaining immature stages

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for rearing. However, none of the females oviposited in these chambers. Species belonging to the Triseriatus Group were collected in four Mexican states (Table 1), two in northeastern Mexico (states of Nuevo León and Tamaulipas), one in central Mexico (Querétaro), and one in the south (Guerrero). The Coastal Plain of the North Gulf extends parallel to the Gulf of Mexico. It exhibits plains and hills, mountains and a coastal line, with a maximum elevation between 1,200-1,400 m above sea level. This region contains subregions of plains and hillsides and San Carlos Sierra, where the predominant vegetation is submontane scrub, thorn scrub, and Forest of Pine-Oak (INEGI 2010). The Sierra Madre Oriental is a mountainous region extending from northeastern Mexico to the states of San Luis Potosí, Hidalgo, Querétaro, Puebla, and Veracruz (INEGI 2010). The subregions of the Grand Folded Sierra and Huasteco Carso have forests of pine-oak, oakpine, and submontane scrub with sub-humid temperate climate and elevations from 600 to 1,200 m above sea level. The Sierra Madre del Sur has subregions such as the South Coast, which extends along the Pacific Ocean, has deciduous forests with humid temperate climate and elevations less than 500 m (INEGI 2010). RESULTS Historic records that report the presence of Ae. triseriatus in Mexican states are: Vargas (1956) in Morelos and Quintana Roo; Díaz-Nájera and Vargas (1973) in Campeche, Nuevo León, Quintana Roo, Tamaulipas and Yucatán; Ibáñez and Martínez (1994) in Campeche, Chihuahua, Coahuila, Morelos, Nuevo León,

Table 1. Physiography of the collection sites and municipalities sampled. Ae. brelandi (b), Ae. triseriatus(t), Ae. zoosophus(z). Region Coastal Plain of North Gulf

Subregion

Vegetation

State

Grand Folded Sierra Sierra Madre Oriental

Nuevo León

Linares Escobedo

Baños de San Ignacio(b) Carretera a Colombia(b)

Submontane Scrub

Tamaulipas

Victoria Palmillas

Ciudad Victoria(z) 6 de Abril(t)

Forest of Pine-Oak

Tamaulipas

Cruillas

El Milagro(b,z)

Santiago

Sierra San Carlos(b,t) Puerto Genovevo(b)

Allende

Paraje del Oso(t) Sierra la Camotera(b) Lazarillos de abajo(t)

Gómez Farías

El Cielo(z)

Juarez

Villa de Juárez(t,z)

San Pedro-Garza García

Chipinque(t)

Jalpan de Serra

Rancho el 99(t) Camino a la Selva(b) Rancho el Lucero(b,t) Rancho el Rodeo(t)

Pinal de Amoles

El Chuveje(t)

Ometepec

Ometepec(z)

Forest of Oak-Pine

Nuevo León

Tamaulipas Submontane Scrub

Huasteco Carso Oak forest

Sierra Madre del Sur South Coast

Location

Thorny Scrub Plains and Hills San Carlos Sierra

Municipality

Deciduous forest

Nuevo León

Querétaro

Guerrero

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Figure 1. Distribution of the Triseriatus Group Species in Mexico. Quintana Roo, Tamaulipas and Yucatán; and Muñoz-Cabrera et al. (2006) in Tlaxcala. The Triseriatus Group species from our records are shown by superscripts in Table 1. DISCUSSION Based on our collection records, Ae. brelandi, Ae. triseriatus, and Ae. zoosophus occur in the Nearctic region of Mexico and Ae. zoosophus occurs also in the Neotropical region. We lack information about where voucher specimens for reports of Ae. triseriatus in tropical areas of Mexico might be kept, but we suspect that the reports refer to other species in the subgenus Protomacleaya. Ae. triseriatus was first reported in the states of Morelos and Quintana Roo by Vargas (1956) and later, taking into account Vargas’ findings, several authors reported its presence in Campeche and Yucatan (Díaz-Nájera and Vargas 1973, Ibáñez and Martínez 1994). However, the specimens from Quintana Roo were identified by Vargas when knowledge of the Mexican species of subgenus Protomacleaya was incomplete. Taxonomy of Protomacleaya was clarified when Schick (1970) and Zavortink (1972) published taxonomic keys for the correct identification of the species. Ae. triseriatus has been reported in northern Mexican states, such as Chihuahua, Coahuila, Nuevo León and Tamaulipas (DíazNájera and Vargas 1973, Ibáñez and Martínez 1994), and there are recent reports of this species in central Mexican states like Morelos (Vargas 1956, Ibáñez and Martínez 1994) and Tlaxcala (Muñoz-Cabrera et al. 2006). These states belong at least in part to the Nearctic region (Figure 1). We consider it possible that Ae. triseriatus might be present in the states of Chihuahua, Coahuila, México, Hidalgo, Morelos, and San Luis Potosí. The first report of Ae. brelandi was made by Zavortink (1972) in the Chisos Mountains, Big Bend National Park in Texas. He hypothesized that the species might occur to the south through the mountainous complexes of the Sierra Madre Oriental. The regions where this species has been reported share climatic and

physiographic similarities with Big Bend National Park. The range of Ae. brelandi in Mexico is parallel to the Gulf of Mexico, through the Coastal Plains of Northern Gulf and of the eastern Sierra Madre Oriental. This species could be present in these regions in the states of Coahuila, San Luis Potosí, Hidalgo, Puebla, and Veracruz (Figure 1). Ae. brelandi represents a new national record for Mexico and the first record outside the United States. Ae. hendersoni has not been reported in Mexico. In northeastern Mexico, Ae. zoosophus had been previously recorded (Vargas 1956, Zavortink 1972, Ibáñez and Martínez 1994, Díaz-Nájera and Vargas 1973, Aguirre et al. 2008, Ortega 2010), and it develops in the same regions and subregions where Ae. brelandi and Ae. triseriatus occur. In 2008 Ae. zoosophus was collected in the coastal forest of Guerrero State, in the Neotropical region; this represents the first confirmed record of any Triseriatus group species outside the Nearctic region. Ae. zoosophus extends from the south central United States through the Sierra Madre Oriental in the Nearctic region, crossing to the Sierra Madre del Sur in the Pacific coast of Guerrero State (Figure 1). In Mexico, species of the Triseriatus group may occur together in various regions and states: in Nuevo León State (Grand Folded Sierra with submontane scrub), Ae. triseriatus and Ae. zoosophus were collected breeding in the same tree hole. Ae. triseriatus breeding in the same tree hole with Ae. zoosophus has been previously reported (Breland 1949, Carpenter and LaCasse 1955, Zavortink 1972). In Tamaulipas State (San Carlos Sierra with submontane scrub), Ae. brelandi and Ae. zoosophus were collected at the same locality and date. Immature stages of Ae. zoosophus were collected in a discarded tire, while Ae. brelandi was collected biting/landing. Also, in the San Carlos Sierra, Ae. brelandi and Ae. triseriatus were simultaneously collected biting/landing. In Queretaro State (Huasteco Carso with oak forest), Ae. brelandi and Ae. triseriatus were collected biting/landing. It is probable that all species breed naturally in tree holes filled with rainwater in the Mexican regions where they occur.

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Midwestern, mid-Atlantic and southeastern states of the United States have had reports of the occurrence of LACV (CDC 2010). There have been well documented positive cases of this disease, and considering the geographical closeness with northern México, entomological surveys for Ae. triseriatus and epidemiological surveys for LACV are strongly recommended to be conducted by Mexican health authorities in states where this species has been reported. In the Gran Folded Sierra and Huasteco Carso subregions of eastern Sierra Madre Oriental, environmental conditions are optimal for the development of this species. If population density of this species increases in rural and suburban localities and villages of these subregions, an epidemiological risk for contracting this disease could also increase. REFERENCES CITED Aguirre, A.U., S.P. Vergara, O.M. García, J.F. Landeros, M.D. Flores, and M.K. Harris. 2008. Culicid distribution in Coahuila, Mexico. Southwest. Entomol. 33: 219-222. Breland, O. P. 1949. Distinctive features of the larvae of Aedes alleni Turner (Diptera: Culicidae). J. N.Y. Entomol. Soc. 57: 93-100. Carpenter, S.J. and W.J. LaCasse. 1955. Mosquitoes of North America (North of Mexico). University of California Press, Berkeley. 360 pp. Darsie, R.F. and R.A. Ward. 2005. Identification and Geographical Distribution of the Mosquitoes of North America, North of Mexico. University Press of Florida. Gainesville, FL. 304 pp. Díaz-Nájera, A. and L. Vargas. 1973. Mosquitos mexicanos distribución geográfica actualizada. Rev. Invest. Salud Pública (México) 33: 111-125. Ibáñez, S.B. and C.C. Martínez. 1994. Clave para la identificación de larvas de mosquitos comunes en las áreas urbanas y

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suburbanas de la República Mexicana (Diptera: Culicidae). Folia Entomol. Mex. 92: 43-73. Instituto Nacional de Estadística y Geografía (INEGI). 2010. Regiones Fisiográficas. México, D.F. [Online] (http://www. inegi.gob.mx) (accssed-9-March- 2012). Muñoz-Cabrera, L .O., S. Ibáñez-Bernal, and M. C. CoronaVargas. 2006. Los mosquitos (Diptera: Culicidae) de Tlaxcala, México. I: Lista comentada de especies. Folia Entomol. Mex. 45: 223-271. Munstermann, L.E., D.B. Taylor, and T.C. Matthews. 1982. Population genetics and speciation in the Aedes triseriatus group. In: W.W.M. Steiner, W.J. Tabachnick, K.S. Rai, and S. Narang (eds.). Recent Developments in the Genetics of Insect Disease Vectors. pp. 433-453. Stipes Publishing Co., Champaign, IL. Ortega, A.M., A.G. Cortés, T.V. Perezgasga, F.R. Sánchez, S.R. Hernández, and I.S. Fernández. 2013. Los mosquitos de Guerrero: región costera (Diptera: Culicidae). Entomol. Mex. 12: 845-849. Schick, R.X. 1970. Mosquito studies (Diptera, Culicidae) XX. The Terrens Group of Aedes (Finlaya). Contrib. Am. Entomol. Inst. 5: 1-158. Taylor, D.B. 1990. Genetics of interspecific hybridization in the Triseriatus and Zoosophus Groups of Aedes (Protomacleaya) (Diptera: Culicidae). Ann. Entomol. Soc. Am. 83: 1181-1191. Vargas, L. 1956. Especies y distribución de mosquitos mexicanos no Anofelinos (Insecta: Diptera). Rev. Inst. Salubr. Enferm. Trop. 15: 19-36. Zavortink, T.J. 1972. Mosquitoes studies (Diptera: Culicidae) XXVIII. The New World species formerly placed in Aedes (Finlaya). Contrib. Am. Entomol. Inst. 8: 1-206.

Geographical distribution of the Aedes Triseriatus Group (Diptera: Culicidae) in Mexico.

Aedes brelandi Zavortink is reported for the first time outside of the United States, where it has been found in northern and central parts of Mexico...
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