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Nova scientia

versión On-line ISSN 2007-0705

Nova scientia vol.12 no.25 León nov. 2020  Epub 17-Feb-2021

https://doi.org/10.21640/ns.v12i25.2651 

Ciencias naturales e ingenierías

New records of mosquito species (Diptera: Culicidae) in La Comarca Lagunera, Durango, Mexico

Nuevos registros de especies de mosquitos (Diptera: Culicidae) de la Comarca Lagunera de Durango, México

Rafael Vázquez-Marroquín1  2  * 

Mónica Duarte-Andrade1 

Luis M. Hernández-Triana3 

Aldo I. Ortega-Morales4 

Rahuel J. Chan-Chable1 

1 Universidad Autónoma Agraria Antonio Narro, Postgrado en Ciencias en Producción Agropecuaria, Unidad Laguna.

2 Instituto de Salud del Estado de Chiapas, Distrito de Salud No. X, Motozintla.

3 Animal and Plant Health Agency, Virology Department, Rabies and Viral Zoonoses (VI1), London.

4 Universidad Autónoma Agraria Antonio Narro, Departamento de Parasitología, Unidad Laguna.


Abstract

Introduction:

Many mosquitoes are of great medical and veterinary importance because they transmit numerous pathogens which cause diseases in animals and humans; thus, knowing their taxonomy and distribution is pivotal for implementing the correct control strategies. The aim of this study was to determine the occurrence of mosquito species and their distribution in La Comarca Lagunera in the state of Durango, Mexico.

Method:

Adult mosquitoes were collected at different resting sites in four municipalities between August and November 2018 using Insectzookas. Aquatic habitats were also sampled for immature stages. Adult specimens were killed using lethal chambers with triethylamine vapors; while larvae and pupae were stored in individual tubes to obtain the adult stages and associated exuviae. All material was transported to the Molecular Biology Laboratory of the Parasitology Department of the Universidad Autónoma Agraria Antonio Narro, Unidad Laguna (UAAAN-UL) for mounting and taxonomical identification. Species were identified using taxonomic keys for the region.

Results:

In total, 689 mosquito specimens (286 males and 403 females) were collected belonging to 15 species, among them Anopheles franciscanus McCracken, Culex erythrothorax Dyar, and Toxorhynchites moctezuma (Dyar and Knab) are new records for Durango State. The most abundant species was Cx. quinquefasciatus Say with 364 (56.2%) specimens, followed by Aedes aegypti (Linnaeus) (21.3%) and Ae. vexans (Meigen) (7.7%).

Conclusion:

13 out of 15 species collected are associated with the transmission of an arbovirus of relevant medical or veterinary importance in Mexico. There are now 38 species recorded for Durango. The information in this study is directly relevant for the Health Ministry in Durango State for the control of vector borne diseases in the region.

Keywords: checklist; distribution; first record; culicides; vectors; Durango; mosquitoes; Comarca Lagunera; Mexico

Resumen

Introducción:

Un número notable de mosquitos tienen gran importancia médica y veterinaria debido a que transmiten numerosos patógenos que causan enfermedades en los animales y los seres humanos, por lo que conocer su taxonomía y distribución es fundamental para aplicar estrategias de control correctas. El objetivo de este estudio fue determinar la presencia de especies de mosquitos y su distribución en la Comarca Lagunera del estado de Durango, México.

Método:

Entre agosto y noviembre de 2018 fueron colectados mosquitos adultos utilizando aspiradores de campo (Insectzookas) en diferentes sitios de reposo en cuatro municipios. También se tomaron muestras de los hábitats acuáticos para la colecta de etapas inmaduras. Los especímenes adultos se mataron utilizando cámaras letales con vapores de trietilamina, mientras que las larvas y las pupas se almacenaron en tubos individuales para obtener los estadios adultos y las exuvias asociadas. Todo el material se transportó al Laboratorio de Biología Molecular del Departamento de Parasitología de la Universidad Autónoma Agraria Antonio Narro, Unidad Laguna (UAAAN-UL) para su montaje e identificación taxonómica. Las especies fueron identificadas usando claves taxonómicas para la región.

Resultados:

En total se colectaron 689 mosquitos (286 machos y 403 hembras) pertenecientes a 15 especies de las cuales Anopheles franciscanus McCracken, Culex erythrothorax Dyar y Toxorhynchites moctezuma (Dyar y Knab) son nuevos registros para el Estado de Durango. La especie más abundante fue Cx. quinquefasciatus Say con 364 (56.2%) especímenes, seguida de Aedes aegypti (Linnaeus) (21.3%) y Ae. vexans (Meigen) (7.7%).

Conclusión:

13 de las 15 especies colectadas están asociadas a la transmisión de algún patógeno de importancia médica o veterinaria en México. Con la adición de los nuevos registros, la lista de mosquitos distribuidos en el estado de Durango alcanza un total de 38 especies. La información generada en este estudio deberá ser útil para la Secretaría de Salud del estado de Durango para el control de las enfermedades transmitidas por mosquitos en la región de la Comarca Lagunera.

Palabras clave: listado; distribución; primer registro; culícidos; vectores; Durango; mosquitos; Comarca Lagunera; México

Introduction

The majority of mosquitoes are hematophagous insects of great medical and veterinary relevance because the females of numerous species can transmit pathogens which cause diseases in animals and humans (Harbach, 2020). Some of these pathogens are arboviruses, for example: Dengue Virus (DENV), Zika Virus (ZIKV), Chikungunya Virus (CHIKV), Yellow Fever Virus (YFV), Western Equine Encephalomyelitis Virus (WEEV) (Liria and Navarro, 2010; Díaz-González et al., 2015; Turell et al., 2015). Mosquitoes causes greater morbidity and mortality in humans than any other groups of organisms (Harbach, 2020). High densities of biting females result in a significant biting issue, especially in touristic areas (Meisch, 1994).

There are 3,578 described mosquito species which are found in most habitats and terrestrial ecosystems (Harbach, 2020); all species are classified in two subfamilies Anophelinae and Culicinae within the Culicidae family, which include approximately 113 genera. In Mexico, there have been 20 genera and approximately 250 species recorded in the country. For Durango State in particular, presently there are only 35 species reported (Vargas, 1956; Vargas and Martínez-Palacios, 1956; Díaz Nájera and Vargas, 1973; Sudia et al., 1975; Duarte-Andrade et al., 2019; Hernández Amparan et al., 2020).

Durango State is situated in the center-northwestern region of Mexico. The weather is warm and dry, but it is temperate and humid during the rainy season (INEGI, 2019). It has a surface of 123,181 km2, placing it as the fourth largest territory in Mexico (INEGI, 2019). In addition, there are five physiographical regions (La Sierra Madre Occidental, Sierras and Northern Plains, Sierra Madre Oriental, Mesa del Centro, and Pacific Coastal Plains), allowing for a high diversity of ecosystems within the State. With the exception of the Evergreen Tropical Forest or High-Altitude Jungle, almost all types of vegetation in Mexico are present in Durango (González Elizondo et al., 2006). Therefore, Durango State has environmental conditions to sustain a high number of mosquito species, including those that have relevant medical and veterinary importance in Mexico.

In the last five years, The Ministry of Health have reported an average of 280 cases of DENV per year, while cases of ZIKV, CHIKV and malaria averaged one per year (DGE, 2019). The presence of cases implies a potential risk of disease growth if conditions are present (López Vélez y Molina Moreno, 2005). On the other hand, cattle farming is one of the key economic activities in northern Durango; especially in the zone known as La Comarca Lagunera. Cattle are affected by the presence of certain species of the genus Psorophora (Robineau-Desvoidy), large mosquitoes that have a marked zoophilic behavior and large densities during the rainy season, causing weight loss and reduction in milk production (Meisch, 1994).

In spite of the critical economic importance of mosquitoes, investigation into mosquitoes in Durango State have been neglected. In our study, we aimed to document occurrence and distribution of mosquito species in seven localities in La Comarca Lagunera, with the aim to update the checklist of culicid species present in the State, which would facilitate the control strategies performed by the Ministry of Health in this region.

Methods

Specimen collection and taxonomic identification

Collection of immature and adult stages were carried out in seven localities: Cañón de Fernández (25°18´24.09”N-103°43´58.09”W), Predio La Isla (25°30´16”N-103°37´24”W), 6 de Enero (25°31´12.97”N-103°35´47.92”W), Gómez Palacio (25°35´42.96”N-103°29´38.95”W), Venecia (25°46´52.12”N-103°21´4.33”W), Bermejillo (25°52´55.97”N-103°37´25.77”W) and Tlahualilo (26°6´29”N-103°26´20.77”W) (Fig. 1). Collection was scheduled between 18:00 and 21:00 hours. These localities belong to four municipalities (Gómez Palacio, Lerdo, Mapimí and Tlahualilo) of La Comarca Lagunera, northeastern Durango, Mexico, which are included in the physiographical region of Sierras and Northern Plains, subregion Bolsón de Mapimí, which include isolated mountains and wide plains where endorheic basins are common (González Elizondo et al., 2006).

Fig. 1 Study area showing the mosquito’s collection sites in Durango State, Mexico. 1 = Cañón de Fernández; 2 = Predio La Isla; 3 = 6 de Enero; 4 = Gómez Palacio; 5 = Venecia; 6 = Bermejillo; and 7 = Tlahualilo. 

Field work was completed between August and November 2018 in the rainy season following the collecting protocol of Belkin et al. (1967). In this case, available water bodies were sampled using dippers and pipettes, while adult mosquitoes were directly collected from resting places or by landing catches using a field aspirator (Insectzookas, BioQuip No. 2888A, Compton, CA). Adult specimens were killed using lethal chambers with triethylamine vapors and stored into vials (Ortega-Morales et al., 2019). All material was transported to the Molecular Biology Laboratory of the Parasitology Department of the Universidad Autónoma Agraria Antonio Narro, Unidad Laguna (UAAAN-UL) for mounting and taxonomical identification. Larvae and pupae were stored on individual tubes to obtain the adult stages and associated exuviae (Ortega-Morales et al., 2010).

Species were identified using the keys of Wilkerson et al. (1990) and Darsie and Ward (2005). All specimens were deposited at the Culicidae Collection of the UAAAN-UL under accession number: 01021018-6E, 01061018-PI, 01071018-B, 01100818-CF, 01121018-V, 01131018-GP, 01160818-T, 01270918-B, and 01310818-6E.

Checklist of the mosquito species in Durango

In order to obtain information about which mosquito species have been previously recorded in Durango, we carried out a literature review in the web pages of “Systematic Catalogue of Culicidae” hosted by the Walter Reed Biosystematics Unit (www.wrbu.org) (WRBU, 2005), the Mosquito Taxonomic Inventory (Harbach, 2020), and other databases such as PubMed Health, BIOSIS, Medline, Zoological Records, GBIF (Global Biodiversity Information Facility) and Google Scholar, using keywords such as “records, mosquitoes, Culicidae, Durango State, Mexico”. The classification criteria of the Family Culicidae proposed by Wilkerson et al. (2015) was followed in the present study.

Results

Morphological identification

In total, 689 mosquitoes were collected (403 females and 286 males) belonging to two subfamilies (Anophelinae and Culicinae), three tribes (Aedini, Culicini and Toxorhynchitini), five genera (Anopheles, Aedes, Psorophora, Culex and Toxorhynchites), nine subgenera (Anopheles, Aedimorphus, Georgecraigius, Ochlerotatus, Stegomyia, Grabhamia, Janthinosoma, Culex and Lynchiella) and 15 species. Of the 15 species, 13 (87%) have relevant medical importance in Mexico (Table 1).

Table 1 Species collected in northeastern Durango, Mexico, and their medical/veterinary importance. 

Species F* M* T* Sampled point* Medical/veterinary importance
Anopheles franciscanus 1 0 1 PI Plasmodium vivax Grassi and Feletti, 1890 laboratory conditions (WRBU, 2005).
Anopheles pseudopunctipennis 2 3 5 PI, CF, V Malaria (Hoffmann, 1989).
Aedes vexans 49 4 53 6E, GP, PI, CF EEEV, WEEV, SLEV, ZIKAV (Turell et al., 2005a; Gendernalik et al., 2017).
Aedes epactius 27 7 34 B, GP JCV, SLEV (Hardy et al., 1980; Heard et al., 1991).
Aedes trivittatus 1 0 1 PI TVTV, Dirofilaria immitis (Leidy, 1856) (WRBU, 2005).
Aedes aegypti 64 83 147 B, GP, T DEN, YF, CHIKV, ZIKAV (Christophers, 1960; Díaz-González et al., 2015;
Chouin Carneiro et al., 2016; WRBU, 2005).
Psorophora columbiae 10 0 10 B, GP RVFV, WNV (Bolling et al., 2005; Turell et al., 2015).
Psorophora signipennis 0 1 1 B WEEV (Crane et al., 1983).
Psorophora ferox 1 1 2 PI Dermatobia hominis (L.), ROCV, VEEV, WEEV, EEEV, ILHV
(Carpenter and LaCasse, 1955; de Souza-Lopes et al., 1981; Mitchell et al., 1987; Kulasekera et al., 2001;
Cupp et al., 2004; Turell et al., 2005b).
Culex coronator 1 0 1 PI Unknown.
Culex erythrothorax 8 0 8 V,T WNV (Goddard et al., 2002).
Culex quinquefasciatus 212 175 387 6E,B,GP,PI,V,T Wuchereria bancrofti (Cobbald, 1877) Seurat, 1921, WEEV, SLEV, WNV, ZIKAV
(Carpenter and LaCasse, 1955; Rutledge et al., 2003; Guedes et al., 2017).
Culex stigmatosoma 0 2 2 6E WNV, SLEV (Goddard et al., 2002; Reisen et al., 2005).
Culex tarsalis 21 7 28 B,GP,PI,V,T WEEV, SLEV (Reeves et al., 1947; WRBU, 2005).
Toxorhynchites moctezuma 6 3 9 PI Without medical importance.

EEEV: Eastern Equine Encephalomyelitis Virus; WEEV: Western Equine Encephalomyelitis Virus; SLEV: St. Louis Encephalitis Virus; ZIKV: Zika Virus; JCV: Jamestown Canyon Virus; TVTV: Trivittatus Virus; DEN: Dengue Virus; YFV: Yellow Fever Virus; CHIKV: Chikungunya Virus; RVFV: Rift Valley Fever Virus; WNV: West Nile Virus; VEEV: Venezuelan Equine Encephalitis Virus; ILHV: Ilheus Virus; ROCV: Rocio Virus.

*F = Female; M = Male; T = Total; V = Venecia; 6E = 6 de Enero; B = Bermejillo; GP = Gómez Palacio; T = Tlahualilo; and CF = Cañón de Fernández.

Culex quinquefasciatus Say with 364 specimens (56.2%) was the most abundant species followed by Ae. aegypti (21.3%) and Ae. vexans (7.7%). Culex quinquefasciatus and Cx. tarsalis Coquillett, were widely distributed across the study area. The former was collected in all localities; while collections in the locality 6 de Enero, unyielded any specimens of the latter species (Table 1). Anopheles (Ano.) franciscanus (McCracken), Cx. (Cul.) erythrothorax Dyar, and Tx. (Lyn.) moctezuma (Dyar and Knab), constitute new records for the culicid fauna in Durango State increasing the number to 38 species (Table 2).

Table 2 Updated checklist of the mosquito species found in Durango State. 

Taxon Previous record
Anopheles (Anopheles)
1. aztecus Hoffman VM
2. eiseni Coquillett VM
3. franciscanus McCraken*
4. pseudopunctipennis Theobald VM
5. punctipennis (Say) VM
Aedes (Aedimorphus)
6. vexans (Meigen) S
Aedes (Georgecraigius)
7. epactius Dyar and Knab DV
Aedes (Lewnielsenius)
8. muelleri Dyar HB
Aedes (Ochlerotatus)
9. angustivittatus Dyar and Knab S
10. campestris Dyar and Knab V
11. nigromaculis (Ludlow) DV
12. sollicitans (Walker) DV
13. trivittatus (Coquillett) S
Aedes (Protomacleaya)
14. schicki Zavortink HB
Aedes (Stegomyia)
15. aegypti (Linnaeus) AR
Haemagogus (Haemagogus)
16. anastasionis Dyar HA
Psorophora (Grabhamia)
17. columbiae (Dyar and Knab) HB
18. signipennis (Coquillett) HB
Psorophora (Janthinosoma)
19. ferox (von Humboldt) DA
Culex (Culex)
20. coronator Dyar and Knab AR
21. erythrothorax Dyar*
22. nigripalpus Theobald AR
23. quinquefasciatus Say DV
24. salinarius Coquillett HA
25. stigmatosoma Dyar DV
26. tarsalis Coquillett S
27. thriambus Dyar DV
Culex (Melanoconion)
28. erraticus Dyar and Knab AR
Culex (Microculex)
29. rejector Dyar and Knab AR
Culex (Neoculex)
30. arizonensis Bohart DV
Lutzia (Lutzia)
31. bigoti (Bellardi) HA
Culiseta (Culiseta)
32. particeps (Adams) DV
33. inornata (Williston) HA
Coquillettidia (Coquillettidia)
34. perturbans Walker AR
Mansonia (Mansonia)
35. indubitans Dyar and Shannon HA
Orthopodomyia
36. kummi Edwards HB
Toxorhynchites (Lynchiella)
37. moctezuma (Dyar and Knab)*
Uranotaenia (Uranotaenia)
38. lowii Theobald HA

V: Vargas, (1956); VM: Vargas and Martínez-Palacios, (1956); DV: Díaz-Nájera and Vargas, (1973); S: Sudia et al. (1975); HB: Heinemann and Belkin, (1977); AR: Ávila-Rodríguez et al. (2013); HA: Hernández-Amparan et al. (2020); DA: Duarte-Andrade et al. (2019).

The new records provided in this study are indicated with an asterisk (*).

Discussion

Distribution of mosquito species in Comarca Lagunera, Durango

In the municipality of Gómez Palacio, seven species of mosquitoes have already been reported (Sudia et al., 1975; Heinemann and Belkin, 1977; Ávila-Rodríguez et al., 2013); two additional species (An. pseudopunctipennis and Cx. erythrothorax) are reported in this study, bringing up the total of nine species in this municipality. In Lerdo, five species were previously recorded (Ávila-Rodríguez et al., 2013; Duarte-Andrade et al., 2019); we found seven additional species in this study (An. franciscanus, An. pseudopunctipennis, Ae. vexans, Ae. trivittatus, Cx. coronator, Cx. tarsalis, and Tx. moctezuma) resulting in 12 species identified. In Mapimí municipality, Ávila-Rodríguez et al. (2013) only four species had been reported. Here we identified three more species (Ps. columbiae, Ps. signipennis, and Cx. tarsalis) resulting in seven species in the area. Until now, the mosquito species in Tlahualilo were unknown. Four species were reported in this study (Table 1), highlighting the importance of continuing entomological surveillance within vector control programs in the country (Azari‐Hamidian et al., 2010; Chan-Chable et al., 2019; Hernández-Triana et al., 2019).

There have been other species recorded in several other municipalities within La Comarca Lagunera in Durango State. For example, the records in Simón Bolivar such as Ae. epactius, Cx. coronator, Cx. quinquefasciatus and Cx. stigmatosoma were recorded by Ávila-Rodríguez et al. (2013), while Ávila-Rodríguez et al. (2013) recorded Ae. aegypti, Ae. epactius, Cx. quinquefasciatus, Cx. stigmatosoma and Cx. tarsalis for San Luis del Cordero. Up to now, there were only 14 species recorded for the area of La Comarca Lagunera from Durango (Sudia et al., 1975; Heinemann and Belkin, 1977; Ávila-Rodríguez et al., 2013; Duarte-Andrade et al., 2019). This study confirms the presence of these species and add other five (An. franciscanus, An. pseudopunctipennis, Ae. trivittatus, Cx. erythrothorax, and Tx. moctezuma) increasing to 19 the number of taxa found in this region.

In general, An. pseudopunctipennis and Ae. aegypti are the most relevant species from a medical point of view found in this study. Anopheles pseudopunctipennis is one of the main malaria vectors in Mexico (Loyola et al., 1991; Santamarina Mijares et al., 1999), with two and three cases being reported by the Ministry of Health in 2015 and 2018 in the study area, respectively (DGE, 2019). Aedes aegypti is the main vector of CHIKV, DENV and ZIKV in Mexico; in Durango state there have been an average of 280 cases of DENV between 2015 to 2019, and two to three cases of CHINK and ZIKV (DGE, 2019). In addition, as mentioned earlier, cattle farming is the most important economic activity in La Comarca Lagunera; thus, it is paramount to carry out further bio surveillance studies of arboviruses in target species such as Ps. columbiae, Ps. signipennis and Cx. quinquefasciatus aimed to determine the pathogens transmitted to livestock in the region. From all species, Cx. quinquefasciatus was the most abundant species with a wider distribution.

Updated checklist of mosquitoes species from Durango

The mosquito species in Durango State is relatively poorly known, and previous have only covered the fauna from few cities and municipalities (Sudia et al., 1975; Heinemann and Belkin, 1977; Ávila-Rodríguez et al., 2013; Duarte-Andrade et al., 2019; Hernández-Amparan et al., 2020). Only eight studies have focused on mosquito fauna in Durango State between 1956 to 2020, in which 12 genera, 20 subgenera and 35 species were reported (Vargas, 1956; Vargas and Martínez-Palacios, 1956; Díaz Nájera and Vargas, 1973; Sudia et al., 1975; Heinemann and Belkin, 1977; Ávila-Rodríguez et al., 2013; Duarte-Andrade et al., 2019; Hernández-Amparan et al., 2020) (Table 2). This study adds three new records in Durango State increasing the number to 38 species. The most biodiverse genera are Culex (11 spp.), Aedes (10 spp.) and Anopheles (5 spp.) (Table 2).

Anopheles franciscanus (McCracken) is distributed across USA and Mexico (WRBU, 2005). In Mexico, this species has been found in the following states: Aguascalientes, Baja California, Baja California Sur, Chiapas, Chihuahua, Coahuila, Hidalgo, Jalisco, Nuevo León, Oaxaca, Quintana Roo, Sonora, Tamaulipas and Zacatecas (Vargas and Martínez Palacios, 1956; Casas Martínez and Orozco Bonilla, 2006; Ortega-Morales et al., 2010; Bond et al., 2014; Ortega-Morales et al., 2015). The females of An. franciscanus are active during the twilight and rarely enters human dwellings to feed as they mainly feed on mammals such as sheep (WRBU, 2005). Larvae were collected in ponds with abundant green algae, swamps with floating aquatic vegetation and metal troughs (Ortega-Morales et al., 2015). Larvae of An. franciscanus were collected in a small stream with dense aquatic vegetation in the recreation area of La Isla. Durango is the fifteenth State in Mexico where An. franciscanus has been found. Therefore, this species has the potential to be widely distributed in northern Mexico.

Culex erythrothorax (Dyar 1907) - This species has been recorded from Colombia, Mexico, Panama and USA (WRBU, 2005). In Mexico, Cx. erythrothorax can be found in Baja California, Colima, Guanajuato, Guerrero, Hidalgo, Mexico city, Mexico State, Michoacán, Nuevo León, Tamaulipas, and Tlaxcala (Díaz Nájera and Vargas, 1973; Muñoz Cabrera et al., 2006; Ortega-Morales et al., 2013; Espinoza-Gómez et al., 2013; Ortega-Morales et al., 2015, 2019). Culex erythrothorax is the main vector of West Nile Virus (WNV) in the region (Goddard et al., 2002). Its larvae have been collected in swamps, while the adults have been caught landing on collecting personnel and resting areas in the shade (Espinoza-Gómez et al., 2013; Ortega-Morales et al., 2019). Utilizing the Insectzooka, five females of Cx. erythrothorax were collected in the locality of Venecia, and three females in Tlahualilo that were resting on the vegetation near animal farms. Durango is the twelfth State where the species is recorded.

Toxorhynchites moctezuma (Dyar and Knab) - This species has a wider distribution, extending from the south of the USA, to Central America (Zavortink and Chaverri, 2009). In Mexico, it has been recorded in the states of Campeche, Guerrero, Hidalgo, Jalisco, Oaxaca, Quintana Roo, San Luis Potosí, Tabasco, Tamaulipas and Veracruz (Heineman and Belkin, 1977; Mis Ávila et al., 2013; Ortega-Morales et al., 2015, 2019). The larva of Tx. moctezuma can develop in tree holes, bamboo internodes, nut shells, and artificial containers (Zavortink and Chaverri, 2009). Despite the females of Tx. moctezuma which are phytophagous, the species is considered a great biological control due to the predatory behavior of its larva, which feed upon other mosquito species (Collins and Blackwell, 2000). In our study, we collected nine larvae of Tx. moctezuma in a discarded tyre containing rainwater, where six females and three males were obtained.

Based upon the current distribution of Tx. moctezuma (Zavortink and Chaverri, 2009), the records of Tx. theobaldi for the states of Chiapas, Michoacán, Morelos and Yucatán (Díaz-Nájera and Vargas, 1973; Villegas-Trejo et al., 2010) belong to Tx. moctezuma. Therefore, Durango becomes the fifteenth state where this species has been collected and it constitutes its northernmost distribution record in Mexico.

Finally, 13 of the 15 species collected in this study are of medical and veterinary importance. The current list of mosquitoes present in the state of Durango reaches a total of 38 species. The information generated in this study should be useful for the Secretary of Health of the State of Durango, Mexico, specifically for the region of La Comarca Lagunera.

Acknowledgments

We thank the Consejo Nacional de Ciencia y Tecnología (CONACyT) for fellowship (No. 719439) awarded to RVM. Funding for LMHT was provided by the UK Department for Environment Food and Rural Affairs (DEFRA), Scottish Government and Welsh Government through grants SV3045, and the EU Framework Horizon 2020 Innovation Grant, European Virus Archive (EVAg, grant no. 653316). We also thank Denise A. Marston, Animal and Plant Health Agency, and Sean W. Prosser, Center for Biodiversity Genomics, University of Guelph, Canada, for reviewing the manuscript.

References

Ávila Rodríguez, V., Pérez Muñoz, R., Márquez Hernández, C., Castañeda Gaytán, G., & Nava Camberos, U. (2013). Diversidad de mosquitos Culícidos en cinco municipios de Durango, México. Entomología Mexicana, 878-882. [ Links ]

Azari-Hamidian, S., Linton, Y. M., Abai, M. R., Ladonni, H., Oshagui, M. A., Hanafi Bojd, A. A., Moosa Kazemi, S. H., Shabkniz, H., Pakari, A., & Harbach, R. E. (2010). Mosquito (Diptera: Culicidae) fauna of the Iradian islands in the Persian Gulf. Journal of Natural History, 44, 15-16. DOI: https://doi.org/10.1080/00222930903437358 [ Links ]

Belkin, J. N., Hogue, C. L., Galindo, P., Aitken, T. H., Schick, R. X., & Powder, W. A. (1967). Estudios sobre mosquitos (Diptera, Culicidae) IIa. Métodos para coleccionar, criar y preservar mosquitos. Contributions of the American Entomological Institute, 2, 22-89. [ Links ]

Bolling, B. G., Kennedy, J. H., & Zimmerman, E. (2005). Seasonal dynamics of four potential West Nile vector species in north-central Texas. Journal of Vector Ecology, 30(2), 186-194. [ Links ]

Bond, J. G., Casas Martínez, M., Quiroz Martínez, H., Novelo Gutiérrez, R., Marina, C. F., Ulloa, A., Orozco Bonilla, A., Muñoz, M., & Williams, T. (2014). Diversity of mosquitoes and the aquatic insects associated with their oviposition sites along the Pacific coast of Mexico. Parasites & Vectors, 7(1), 41. [ Links ]

Carpenter, S. J., & LaCasse, W. J. (1955). Mosquitoes of North America (North of Mexico). University of California Press. [ Links ]

Casas Martínez, M., & Orozco Bonilla, A. (2006). Diversidad y distribución geográfica del género Anopheles en el sur de México. CONABIO. Biodiversitas, 67, 12-15. [ Links ]

Chan-Chable, R. J., Martínez Arce, A., Mis Ávila, P. C., & Ortega-Morales, A. I. (2019). DNA barcodes and evidence of cryptic diversity of anthropophagous mosquitoes in Quintana Roo, Mexico. Ecology and Evolution, 9(8), 4692-4705. DOI: https://doi.org/10.1002/ece3.5073 [ Links ]

Christophers, S. R. (1960). Aedes aegypti (L.): the yellow fever mosquito. Cambridge University Press. [ Links ]

Chouin Carneiro, T., Vega Rua, A., Yebakima, A., Girod, R., Goindin, D., Dupont Rouzeyrol, M., Lourenço de Oliveira, R., & Failoux, A. B. (2016). Differential susceptibilities of Aedes aegypti and Aedes albopictus from the America to Zika virus. Plos Neglected Tropical Diseases, 10(3), e0004543. DOI: https://doi.org/10.1371/journal.pntd.0004543. [ Links ]

Collins, L. E., Blackwell, A. (2000). The biology of Toxorhynchites mosquitoes and their potential as biocontrol agents. Biocontrol News and Information, 21(4), 105N-116. [ Links ]

Crane, G. T., Elbel, R. E., Bruce Francy, D., & Calisher, C. H. (1983). Arboviruses from western Utah, USA, 1967 - 1976. Journal of Medical Entomology, 20(3), 294-300. DOI: https://doi.org/10.1093/jmedent/20.3.294 [ Links ]

Cupp, E. W., Zhang, D., Yue, X., Cupp, M. S., Guyer, C., Sprenger, T. R., & Unnasch, T. R. (2004). Identification of reptilian and amphibian blood meals from mosquitoes in an eastern equine encephalomyelitis virus focus in central Alabama. The American Journal of Tropical Medicine and Hygiene, 71(3), 272-276. DOI: https://doi.org/10.4269/ajtmh.2004.71.272 [ Links ]

Darsie, R. F., & Ward, R. A. (2005). Identification and geographical distribution of the mosquitoes of North America, north of Mexico. Gainesville. [ Links ]

de Souza-Lopes, O., Abreu-Sacchetta, L., Francy, D. B., Jacob, W. L., & Calisher, C. H. (1981). Emergence of a new arbovirus disease in Brazil: III. Isolation of Rocio virus from Psorophora ferox (Humboldt, 1819). American Journal of Epidemiology, 113(2), 122-125. DOI: https://doi.org/10.1093/oxfordjournals.aje.a113075 [ Links ]

Dirección General de Epidemiología [DGE] (2019). Epidemiológico, B. Secretaría de Salud de México. [2019-10-21] Available from: Available from: https://www.gob.mx/salud/acciones-y-programas/direccion-general-de-epidemiologia-boletin-epidemiologico . [ Links ]

Díaz-González, E. E., Kautz, T. F., Dorantes Delgado, A., Malo García, I. R., Laguna Aguilar, M., Langsjoen, R., Chen, R., Auguste, D. I., Sánchez Casas, R. M., Danis Lozano, R., Weaber, S., & Fernández Salas, I. (2015). First report of Aedes aegypti transmission of chikungunya virus in the Americas. The American Journal of Tropical Medicine and Hygiene, 93(6), 1325-1329. DOI: https://doi.org/10.4269/ajtmh.15-0450 [ Links ]

Díaz Nájera, A., & Vargas, L. (1973). Mosquitos mexicanos: distribución geográfica actualizada. Revista de Investigación en Salud Pública, 33, 111 - 125. [ Links ]

Duarte-Andrade, M., Vázquez Marroquín, R., Chan-Chablé, R. J., Siller Rodríguez, Q. K., Sánchez Ramos, F. J., Valdés Perezgasga, M. T., González Acosta, C., Correa Morales, F., & Ortega-Morales, A. I. (2019). First record of Psorophora ferox in Durango State, Mexico. Journal of the American Mosquito Control Association, 35(3), 217-219. DOI: https://doi.org/10.2987/19-6822.1 [ Links ]

Espinoza Gómez, F., Arredondo Jiménez, J. I., Maldonado Rodríguez, A., Pérez Rentería, C., Newton Sánchez, O. A., Chávez Flores, E., & Gómez Ibarra, E. (2013). Distribución geográfica de mosquitos adultos (Diptera: Culicidae) en áreas selváticas de Colima, México. Revista Mexicana de Biodiversidad, 84(2), 685-689. DOI: https://doi.org/10.7550/rmb.27184 [ Links ]

Gendernalik, A., Weber Lucarelli, J., Garcia Luna, S., Fauver, J. R., Rückert, C., Murrieta, R. A., Bergen, N., Samaras, D., Nguyen, C., Kading, R. C., & Ebel, G. D. (2017). American Aedes vexans mosquitoes competent vectors of zika virus. The American Journal of Tropical Medicine and Hygiene, 96(6), 1338 - 1340. DOI: https://doi.org/10.4269/ajtmh.16-0963 [ Links ]

Goddard, L. B.; Roth, A. E., & Reisen, W. K. (2002). Vector competence of California mosquitoes for West Nile Virus. Emerging Infectious Diseases, 8(12), 1385-1391. DOI: 10.3201/eid0812.020536. [ Links ]

González Elizondo, M. S., González Elizondo, M., & Márquez Linares, M. A. (2006). Vegetación y ecorregiones de Durango. Plaza y Valdés. [ Links ]

Guedes, D. R. D., Paiva, M. H. S., Donato, M. M. A., Barbosa, P. P., Krokovsky, L., Rocha, S. W. S., Saraiva, K. L. A., Crespo, M. M., Rezende, T. M. T., Wallau, G. L., Barbosa, R. M. R., Oliveira, C. M. F., Melo Santos, M. A. V., Pena, L., Cordeiro, M. T., Franca, R. F. O., Oliveira, A. L. S., Peixoto, C. A., Leal, W. S., & Ayres, C. F. J. (2017). Zika virus replication in the mosquito Culex quinquefasciatus in Brazil. Emerging Microbes & Infections, 6(1), 1-11. DOI: 10.1038/emi.2017.59 [ Links ]

Harbach, R. E. (2020). Mosquito taxonomic inventory. [2020-08-10]. En En http://mosquito-taxonomic-inventory.info/simpletaxonomy/term/6045Links ]

Hardy, J. L., Rosen, L., Kramer, L. D., Presser, S. B., Shroyer, D. A., & Turell, M. J. (1980). Effect of rearing temperature on transovarial transmission of St. Louis encephalitis virus in mosquitoes. The American Journal of Tropical Medicine and Hygiene, 29(5), 963-968. DOI: https://doi.org/10.4269/ajtmh.1980.29.963 [ Links ]

Heard, P. B., Zhang, M., & Grimstad, P. R. (1991). Laboratory transmission of Jamestown Canyon and snowshoe hare viruses (Bunyaviridae: Califormia serogroup) by several species of mosquitoes. Journal of the American Mosquito Control Association, 7(1), 94-102. [ Links ]

Heinemann, S. J., & Belkin, J. (1977). Collection Records of the Project “Mosquitoes of Middle America” 9. Mexico (MEX, MF, MT, MX). Mosquito Systematics, 9(4), 483-535. [ Links ]

Hernández-Amparan, S., Pérez-Santiago, G., Ibáñez-Bernal, S., Hinojosa-Ontiveros, G. A., & Álvarez-Zagoya, R. (2020). Actualización de la riqueza de especies de mosquitos en el Estado de Durango, México. Southwestern Entomologist, 45(1), 251-262. DOI: https://doi.org/10.3958/059.045.0126 [ Links ]

Hernández-Triana, L. M., Brugman, A., Nikolova, N. I., Ruiz Arredondo, I., Barrero, E., Thorne, L., Fernández de Marco, M., Krüger, A., Lumley, S., Johnson, N., & Fooks, A. R. (2019). DNA barcoding of British mosquitoes (Diptera, Culicidae) to support species identification, discovery of cryptic genetic diversity and monitoring invasive species. ZooKeys, 832, 57-76. DOI:10.3897/zookeys.832.32257 [ Links ]

Hoffmann, C. C. (1989). Anopheles pseudopunctipennis y su relación con el paludismo en la República Mexicana. Salud Pública de México, 31(6), 823-832. [ Links ]

INEGI [Instituto Nacional de Estadística y Geografía]. (2019). Anuario Estadístico del Estado de Durango. [2020-08-10]. En En https://www.inegi.org.mx/Links ]

Kulasekera, V. L., Kramer, L., Nasci, R. S., Mostashari, F., Cherry, B., Trock, S. C, Glaser, C., & Miller, J. R. ( 2001). West Nile virus infection in mosquitoes, birds, horses and humans, Staten Island, New York, 2000. Emerging Infectious Diseases, 7(4), 722-725. DOI: 10.3201/eid0704.010421 [ Links ]

Liria, J., & Navarro, J. C. (2010). Modelo de nicho ecológico en Haemagogus Williston (Diptera: Culicidae), vectores del virus de la fiebre amarilla. Revista Biomédica, 21, 149-161. [ Links ]

López-Vélez, R. & Molina Moreno, R. (2005). Cambio climático en España y riesgo de enfermedades infecciosas y parasitarias transmitidas por artrópodos y roedores. Revista Española de Salud Pública, 79(2), 177-190. [ Links ]

Loyola, E. G., Arredondo, J. I., Rodríguez, M. H., Brown, D. N., & Vaca Marin, M. A. (1991). Anopheles vestitipennis, the probable vector of Plasmodium vivax in the Lacandon forest of Chiapas, México. Transactions Royal Society of Tropical Medicine and Hygiene, 85(2), 171-174. [ Links ]

Mitchell, C. J., Monath, T. P., Sabattini, M. S., Daffner, J. F., Cropp, C. B., Calisher, C. H, Darsie Jr, R. F., & Jakob, W. L. (1987). Arbovirus, isolations from mosquitoes collected during and after the late 1982-1983 epizootic of western equine encephalitis in Argentina. The American Journal of Tropical Medicine and Hygiene, 36(1), 107-113. DOI: https://doi.org/10.4269/ajtmh.1987.36.107 [ Links ]

Meisch, M. V. (1994). The dark ricefield mosquito Psorophora columbiae. Wing Beats, 5, 8 [ Links ]

Mis Ávila, P., Canul Amaro, G., & Domínguez Galera, M. A. (2013). Determinación taxonómica de mosquitos (Culicinae: Culicidae) de la zona urbana de Chetumal, Quintana Roo. Revista Salud Quintana Roo, 6(23), 8-13. [ Links ]

Muñoz-Cabrera, L. O., Ibáñez Bernal, S., & Corona Vargas, M. C. (2006). Los mosquitos (Diptera: Culicidae) de Tlaxcala, México. I: Lista comentada de especies. Folia Entomológica Mexicana, 45(3), 223-271. [ Links ]

Ortega-Morales, A. I., Mis Ávila, P., Elizondo Quiroga, A., Harbach, R. E., & Siller Rodríguez, Q. K. (2010). The mosquitoes of Quintana Roo State, Mexico (Diptera: Culicidae). Acta Zoológica Mexicana, 26(1), 33-46. [ Links ]

Ortega-Morales, A. I., Cortés Guzmán, A. J., Valdés Perezgasga, M. T., Sánchez Ramos, F. J., Hernández Rodríguez, S., & Fernández Salas, I. (2013). Los mosquitos de Guerrero: Región costera (Diptera: Culicidae). Entomología Mexicana, 12, 845-849. [ Links ]

Ortega-Morales, A. I., Zavortink, T. J., Huerta Jiménez, H., Sánchez Ramos, F. J., Valdés Perezgasga, M. T., Reyes Villanueva, F., Siller Rodríguez, Q. K., & Fernández Salas, I. (2015). Mosquito records from Mexico: the mosquitoes (Diptera: Culicidae) of Tamaulipas State. Journal of Medical Entomology, 52(2), 171-184. DOI: 10.1093/jme/tju008 [ Links ]

Ortega-Morales, A. I., Zavortink, T., Huerta Jiménez, H., Ibáñez Bernal, S., & Siller Rodríguez, Q. K. (2019). The mosquitoes (Diptera: Culicidae) of Hidalgo state, Mexico. Acta Tropica, 189, 94-103. DOI: 10.1016/j.actatropica.2018.07.003 [ Links ]

Reeves, W. V., Mack, W. N., & Hammon, W. M. (1947). Epidemiological Studies on Western Equine Encephalomyelitis and St. Louis encephalitis in Oklahoma, (1944). The Journal of Infectious Diseases, 81(2), 191-196. [ Links ]

Reisen, W. K., Fang, Y., & Martínez, V. M. (2005). Avian host and mosquito (Diptera: Culicidae) vector competence determine the efficiency of West Nile and St. Louis encephalitis virus transmission. Journal of Medical Entomology, 42(3), 367-375. DOI: https://doi.org/10.1093/jmedent/42.3.367 [ Links ]

Rutledge, C. R., Day, J. F., Lord, C. C., Stark, L. M., & Tabachnick, W. J. (2003). West Nile virus infection rates in Culex nigripalpus (Diptera: Culicidae) do not reflect tranmission rates in Florida. Journal of Medical Entomology, 40(3), 253-258. DOI: https://doi.org/10.1603/0022-2585-40.3.253 [ Links ]

Santamarina Mijares, A., Pérez Pacheco, R., Tomás Martínez, S. H., Cantón, L. E., & Flores Ambrosio, G. (1999). The Romanomermis iyengari parasite for Anopheles pseudopunctipennis suppression in natural habitats in Oaxaca State, Mexico. Revista Panamericana de Salud Pública, 5, 23-28. [ Links ]

Sudia, W. D., Fernández, L., Newhouse, V. F., Sanz, R., & Calisher, C. H. (1975). Arbovirus vector ecology studies in Mexico during the 1972 Venezuelan equine outbreak. American Journal of Epidemiology, 101(1), 51-58. DOI: 10.1093/oxfordjournals.aje.a112070 [ Links ]

Turell, M. J., Britch, S. C., Aldridge, R. L., Xue, R. D., Smith, M. L., Cohnstaedt, L. W., & Linthicum, K. J. (2015). Potential for Psorophora columbiae and Psorophora ciliata Mosquitoes (Diptera: Culicidae) to Transmit Rift Valley Fever Virus. Journal Medical Entomology, 52(5), 1111-1116. DOI: https://doi.org/10.1093/jme/tjv093 [ Links ]

Turell, M. J, Dohm, D. J., Sardelis, M. R., O´guinn, M. L., Andreadis, T. G, & Blow, J. A. (2005a). An update on the potential of North American mosquitoes (Diptera: Culicidae) to transmit West Nile virus. Journal Medical Entomology, 42(1), 57-62. DOI: https://doi.org/10.1093/jmedent/42.1.57 [ Links ]

Turell, M. J., O´guinn, M. L., Jones, J. W., Sardelis, M. R., Dohm, D. J., Watts, D. M., Fernández, R., Travassos Da Rosa, A., Guzman, H., Tesh, R., Rossi, C. A., Ludwig, G. V., Mangiafico, J. A., Kondig, J., Wasieloski Jr, L. P., Pecor, J., Zyzak, M., Schoeler, G., Mores, C. N., Calampa, C., Lee, J. S., & Klein, T. A. (2005b). Isolation of viruses from mosquitoes (Diptera: Culicidae) collected in the Amazon Basin Region of Peru. Journal Medical Entomology, 42(5), 891-898. DOI: https://doi.org/10.1093/jmedent/42.5.891 [ Links ]

Vargas, L. (1956). Especies y distribución de mosquitos mexicanos no anofelinos (Insecta Diptera). Revista del Instituto de Salubridad y Enfermedades Tropicales, 16(1), 19-36. [ Links ]

Vargas, L., & Martínez Palacios, A. (1956). Anofelinos mexicanos taxonomía y distribución. Secretaria de Salubridad y Asistencia, Comisión Nacional para la Erradicación del Paludismo, México. [ Links ]

Villegas-Trejo, A., Manrique Saide, P., Che Mendoza, A., Cruz Canto, W., González Fernández, M., González Acosta, C., Dzul Manzanilla, F., Huerta, H., & Arredondo Jiménez, J. I. (2010). First report of Aedes albopictus and other mosquito species in Morelos, Mexico. Journal of the American Mosquito Control Association, 26(3), 321-323. DOI: https://doi.org/10.2987/10-6014.1 [ Links ]

WRBU [Walter Reed Biosystematics Unit]. (2005). Systematic Catalog of Culicidae. [Internet]. Suitland, MD: WRBU [2020-08-10]. En En http://www.mosquitocatalog.org . [ Links ]

Wilkerson, R. C., Linton, Y. M., Fonseca, D. M., Schultz, T. R., Price, D. C., & Strickman, D. A. (2015). Making mosquito taxonomy useful: a stable classification of tribe Aedini that balances utility with current knowledge of evolutionary relationships. PLoS One. DOI: https://doi.org/10.1371/journal.pone.0133602 [ Links ]

Wilkerson, R. C., Strickman, D. A., & Litwak, T. R. (1990). Illustrated key to the female anopheline mosquitoes of Central America and Mexico. Journal of the American Mosquito Control Association, 6(1), 7-34. [ Links ]

Zavortink, T. J., & Chaverri, L. G. (2009). Resurrection of the names Toxorhynchites moctezuma (Dyar and Knab) and Toxorhynchites hypoptes (Knab) from synonymy with Toxorhynchites theobaldi (Dyar and Knab) (Diptera: Culicidae). Proceedings of the Entomological Society of Washington, 111(4), 890-898. DOI: http://dx.doi.org/10.4289/0013-8797-111.4.890 [ Links ]

Received: August 10, 2019; Accepted: September 25, 2020

Autor para correspondencia: Rafael Vázquez-Marroquín, E-mail: vamara23@hotmail.com

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