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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.
