First record of Limatus durhamii Theobald (Diptera: Culicidae) in Campeche, Mexico

Abstract

A total of 194 specimens were collected (160 larvae, 34 pupae) representing 6 species from 4 genera (Aedes aegypti, Ae. scapularis, Culex coronator, Cx. nigripalpus, Haemagogus anastasionis, and Limatus durhamii). In the study, a total of 18 larvae of Li. durhamii (9.28%) were collected in natural and artificial breeding sites in the municipalities of Campeche (3), Escárcega (6), Hecelchakán (6), and Tenabo (3). We report here the first collection record of Li. durhamii for the state of Campeche in southern Mexico. Further studies are necessary to investigate the geographic distribution of Li. durhamii throughout the country.

Alternate abstract:

Un total de 194 ejemplares fueron recolectados (160 larvas, y 34 pupas) lo que representa 6 especies pertenecientes a 4 géneros (Aedes aegypti, Ae. scapularis, Culex coronator, Cx. nigripalpus, Haemagogus anastasionis y Limatus durhamii). En el estudio, un total de 18 larvas de Li. durhamii (9,28%) fueron recolectadas en criaderos naturales y artificiales en los municipios de Campeche (3), Escárcega (6), Hecelchakán (6) y Tenabo (3), ver mapa. Con esto, se corrobora la presencia de 5 especies de mosquitos pertenecientes a 3 géneros, e informamos del primer registro de colecta de Li. durhamii para el estado de Campeche, en el sur de México. Este registro amplía la distribución geográfica de Li. durhamii en México que puede estar implicado como vector en los ciclos de transmisión de arbovirosis endémicos. Se necesitan estudios adicionales para investigar la distribución geográfica de Li. durhamii en todo el país.

Headnote

Summary

A total of 194 specimens were collected (160 larvae, 34 pupae) representing 6 species from 4 genera (Aedes aegypti, Ae. scapularis, Culex coronator, Cx. nigripalpus, Haemagogus anastasionis, and Limatus durhamii). In the study, a total of 18 larvae of Li. durhamii (9.28%) were collected in natural and artificial breeding sites in the municipalities of Campeche (3), Escárcega (6), Hecelchakán (6), and Tenabo (3). We report here the first collection record of Li. durhamii for the state of Campeche in southern Mexico. Further studies are necessary to investigate the geographic distribution of Li. durhamii throughout the country.

Key Words: Mosquitoes, Limatus, Orthobunyavirus

Sumario

Un total de 194 ejemplares fueron recolectados (160 larvas, y 34 pupas) lo que representa 6 especies pertenecientes a 4 géneros (Aedes aegypti, Ae. scapularis, Culex coronator, Cx. nigripalpus, Haemagogus anastasionis y Limatus durhamii). En el estudio, un total de 18 larvas de Li. durhamii (9,28%) fueron recolectadas en criaderos naturales y artificiales en los municipios de Campeche (3), Escárcega (6), Hecelchakán (6) y Tenabo (3), ver mapa. Con esto, se corrobora la presencia de 5 especies de mosquitos pertenecientes a 3 géneros, e informamos del primer registro de colecta de Li. durhamii para el estado de Campeche, en el sur de México. Este registro amplía la distribución geográfica de Li. durhamii en México que puede estar implicado como vector en los ciclos de transmisión de arbovirosis endémicos. Se necesitan estudios adicionales para investigar la distribución geográfica de Li. durhamii en todo el país.

Palabras Clave: Mosquitos, Limatus, Orthobunyavirus

Limatus Theobald (Diptera: Culicidae) is a genus of forest mosquito that occurs in Central America, eastern South America, and the West Indies. It is placed in the tribe Sabethini of subfamily Culicinae. Immature stages develop in bamboo cavities, tree holes, fallen bracts, coconut husks, cacao pods, and also in other small water containers such as fallen leaves and spathes, snail shells, rock holes, and a variety of small artificial containers (Lane 1953; Calderón-Arguedas et al. 2009; Campos et al. 2011; Baak-Baak et al. 2014; Mangudo et al. 2017). Currently 9 valid species of Limatus Theobald are recognized, all with Neotropical distribution. In Mexico, 2 species have been recorded, Limatus asulleptus (Theobald) (Ortega-Morales et al. 2015) and Limatus durhamii Theobald (DíazNájera & Vargas 1973). Limatus durhamii can be found with the synonyms of Simondella curvirostris Laveran, Dendromyia paraensis Theobald, Limatus cacophrades Dyar & Knab, and Limatus exhibitor Shannon & Del Ponte, and is a suspected vector of the genus Orthobunyavirus (subfamily: Bunyaviridae) (Berger 2016). The genus Orthobunyavirus includes about 53 species containing more than 193 viruses, grouped into about 20 serogroups based on antigenic relationships, and the majority of the viruses distributed worldwide that are transmitted by mosquitoes but are not well studied (Elliott & Blakqori 2011; Plyusnin et al. 2012), except those that have medical (e.g., La Crosse and Oropouche viruses) or veterinary importance (e.g., the newly emerged Schmallenberg virus).

In Mexico, Li. durhamii has been recorded in the states of Chiapas, Guerrero, Oaxaca, Puebla, San Luis Potosí, and Yucatán (DíazNájera & Vargas 1973; Casas-Martínez & Orozco-Bonilla 2006), Quintana Roo (Pletsch 1986; Ortega-Morales et al. 2010), Tamaulipas (Ortega-Morales et al. 2015), Tabasco, and Veracruz (Heinemann & Belkin 1977).

Immature stages were collected in 4 municipalities of the state (Campeche, Escárcega, Hecelchakán, and Tenabo) from natural breeding sites outside houses, and all water sources were checked from Jan to Dec 2015 Mosquito larvae were collected each mo for 3 consecutive d in the morning, for a total collection effort of 36 days. The larvae were transported alive in plastic bags to the Public Health Laboratory of Campeche State. The collections were conducted in both the dry and rainy seasons. Entomological capture is an activity of the epidemiologic surveillance developed by the Secretary of Health of Mexico.

Taxonomic determinations of immature mosquitoes were based on morphological characteristics of fourth instar larvae using taxonomic keys (Carpenter & LaCasse 1955; Ibáñez-Bernal & MartinezCampos 1994) at the Secretary of Health of Campeche, Mexico, followed by confirmation from the Institute for Diagnostic and Epidemiological Reference. A voucher collection of mosquito larvae was deposited in the Public Health Laboratory of Campeche State.

A total of 194 specimens were collected (160 larvae, 34 pupae) representing 6 species belonging to 4 genera (Aedes aegypti (L.), Ae. scapularis (Rondani), Culex coronator Dyar & Knab, Cx. nigripalpus Theobald, Haemagogus anastasionis Dyar, and Li. durhamii). A total of 18 mosquito larvae of Li. durhamii (9.28%) were collected in natural and artificial breeding sites in the municipalities of Campeche (3: 19.87434°N, 90.47324°W), Escárcega (6: 18.61466°N, 90.73309°W, and 19.00915°N, 91.28392°W), Hecelchakán (6: 20.12974°N, 90.18111°W, and 20.17465°N, 90.14391°W), and Tenabo (3: 20.0344°N, 90.22798°W) for the first time in the state (Fig. 1). Species collected during the study, and the places where they were found, are listed below (Table 1).

Currently, 50 mosquito species have been recorded in Campeche State. This study adds Limatus durhamii to the mosquito fauna record of Campeche with collections in 4 municipalities of the state. Diseases transmitted by arthropods have shown recent changes in dissemination, either by the intercontinental movement of different strains of etiologic agents, the introduction of vectors and exotic reservoirs, or by the susceptible human population that migrates towards endemic areas (Rueda & Hernández 2008). Faunistic studies are necessary to gain information not only of the vector and host species present in the zone, but to recognize their breeding sites, and the environmental factors that determine their presence in the different ecosystems and seasons. Mosquito studies are important for adopting appropriate health measures to control the diseases they transmit, in accordance with the vector species, their abundance, and the time of year favoring the transmission of pathogenic agents. These studies also allow detection of exotic species in a given region (Keesing 2010).

Ochoa-Gómez et al. (2012) mention that distribution of mosquitoes can change due to occupation of new habitats following anthropogenic activities that generate disturbances in the environment. This new record of Li. durhamii in municipalities for the state of Campeche possibly affirms the comment of Berti (2012), who mentioned that there are many factors that can accelerate the emergence of vector-borne diseases, including environmental changes, habitat modifications, variations of human and animal demography, deterioration of strategies of vector control, or changes in pathogen genetics. These factors contribute to the depletion of the abundance and distribution of many species, whereas others have increased explosively to become pests (Peña & Neyra 1998).

The main focus of the surveillance of culicid mosquitoes has been on the genera Aedes, Anopheles, and Culex, with emphasis on geographic distribution and other aspects relevant to the implementation of control activities (Rodriguez & De La Hoz 2005) due to the importance of these species on public health. However, there has been less research on other genera, possibly due to their lower epidemiological impact (Barreto et al. 1996) and transmission of arboviruses (Gubler 2002), as is the case of the mosquitoes in the genus Limatus.

Honório et al. (2006) and Talaga et al. (2017) mentioned that species of Limatus have been found with a high rate of prevalence in artificial water containers along with mosquitoes of Aedes, and reported an interspecific competition with native species for food. Likewise, Ortega-Morales et al. (2010) mentioned that Li. durhamii immatures were observed preying on Ae. aegypti larvae. These mosquito species larvae are saprophagous, and in the absence of decaying matter they can behave like facultative predators of other mosquito species (Lopes 1999). In a study conducted in Costa Rica, Li. durhamii was reported living with Ae. aegypti in the same artificial containers (Marín et al. 2009). Berger (2016) mentioned that mosquitoes of the genus Limatus are potential vectors of Orthobunyaviruses, and Berti et al. (2015) mention that they are potential vectors of arbovirus.

This study documents for the first time the occurrence of Limatus durhamii in the state of Campeche. Further studies are necessary to investigate the establishment of L. durhamii elsewhere in the country and its potential to transmit arboviruses.

We are grateful to the National Council of Science of Technology (Mexico) for project 1072 of Catedras-CONACYT, and to the Ph.D. candidate Sergio Padilla from CEDESU-UAC-Campeche for making the maps.

Footnote

* Corresponding author; E-mail: [email protected]

References

References Cited

Baak-Baak CM, Arana-Guardia R, Cigarroa-Toledo N, Puc-Tinal M, CobaTún C, Rivero-Osorno V, Lavalle-Kantun D, Loroño-Pino MA, MachainWilliams C, Reyes-Solis GC, Beaty BJ, Eisen L, García-Rejón JE. 2014. Urban Mosquito Fauna in Mérida City, México: Immatures Collected from Containers and Storm-water Drains/Catch Basins. NIH Public Access 39: 291-306.

Barreto M, Burbano ME, Suárez M, Barreto P. 1996. Psorophora ciliata y otros mosquitos (Diptera: Culicidae) en Yolombó, Antioquia, Colombia. Colombia Médica 27: 62-65.

Berger S. 2016. Infectious Diseases of the World. GIDEON Informatics Inc., Los Angeles, California, USA.

Berti JA. 2012. Mosquitos (Diptera: Culicidae) de la Gran Sabana, Venezuela. Editorial Académica Española, Spain.

Berti J, Guzmán H, Estrada Y, Ramírez R. 2015. New records of mosquitoes (Diptera: Culicidae) from Bolívar State in South Eastern Venezuela, with 27 new species for the state and 5 of them new in the country. Frontiers in Public Health 2: 268. doi: 10.3389/fpubh.2014.00268

Calderón-Arguedas O, Troyo A, Solano ME, Avendaño A. 2009. Culicid fauna associated to artificial containers in the neighborhood "La Carpio," Costa Rica. Revista Costarricense de Salud Publica 18: 30-36.

Campos RE, Spinelli G, Mogi M. 2011. Culicidae and Ceratopogonidae (Diptera: Nematocera) inhabiting phytotelmata in Iguazú National Park, Misiones Province, subtropical Argentina. Revista de la Sociedad Entomológica Argentina 70: 111-118.

Carpenter SJ, Lacasse WJ. 1955. Mosquitoes of North America (North of Mexico). University of California Press, Berkeley, California, USA.

Casas-Martínez M, Orozco-Bonilla A. 2006. Diversidad y distribución geográfica del género Anopheles en el sur de México. CONABIO, Biodiversitas 67: 12-15.

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

Elliott RM, Blakqori G. 2011. Molecular biology of orthobunyaviruses, pp. 1-39 In Plyusnin A, Elliott RM [eds.], Bunyaviridae: Molecular and Cellular Biology. Caister Academic, Norfolk, United Kingdom.

Gubler DJ. 2002. The global emergence/resurgence of arboviral diseases as public health problems. Archives of Medical Research 33: 330-342.

Heinemann SJ, Belkin JN. 1977. Collection records of the project "Mosquitoes of Middle America" 9. Mexico (MEX, MF, MT, MX). Mosquito Systematics 9: 483-534.

Honório NA, Cabello PH, Codeço CT, Lourenço-de-Oliveira R. 2006. Prelimi-nary data on the performance of Aedes aegypti and Aedes albopictus immature developing in water-filled tires in Rio de Janeiro. Memórias do Instituto Oswaldo Cruz 101: 225-228.

Ibáñez-Bernal S, Martínez-Campos C. 1994. Clave para la identificación de larvas de mosquitos comunes en las áreas urbanas y suburbanas de la República Mexicana (Diptera: Culicidae). Folia Entomologica Mexicana 92: 43-73.

Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS. 2010. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468: 647-652.

Lane J. 1953. Neotropical Culicidae, Vol. I & Vol. II. Sao Paulo, Brasil.

Lopes J. 1999. Ecologia de mosquitos (Diptera Culicidae) em criadouros naturais e artificiais de área rural do norte do Paraná, Brasil. VIII. Influencia das larvas predadoras (Toxorhynchites sp., Limatus durhamii e Culex bigoti) sobre a populacao de larvas de Culex quinquefasciatus e Culex eduardoi. Revista Brasileira de Zoologia 16: 821-826.

Mangudo C, Campos RE, Rossi GC, Gleiser RM. 2017. Snail shells as larval habitat of Limatus durhamii (Diptera: Culicidae) in the Yungas of Argentina. Acta Tropica 167: 204-207.

Marín R, Marquetti MC, Álvarez Y, Gutiérrez JM, González R. 2009. Especies de mosquitos (Diptera: Culicidae) y sus sitios de cría en la región Huetar Atlántica, Costa Rica. Revista Biomédica 20: 15-23.

Ochoa-Gómez L, Barajas-Galindo J, Torres-Gutiérrez C, Uribe-Soto S, Porter C, Vélez-Bernal ID. 2012. Variabilidad genética de mosquitos del género Culex (Diptera: Culicidae) provenientes de diferentes altitudes en la región cafetera de Colombia. Actualidades Biologicas 34: 133-176.

Ortega-Morales AI, Avila P, Elizondo-Quiroga A, Harbach RE, Siller-Rodríguez QK, Fernández-Salas I. 2010. The mosquitoes of Quintana Roo State, Mexico (Diptera: Culicidae). Acta Zoológica Mexicana 26: 33-46.

Ortega-Morales AI, Zavortink TJ, Huerta-Jiménez H, Sánchez-Ramos FJ, Valdéz-Pérezgasca T, Reyes-Villanueva F, Siller-Rodríguez QK, FernándezSalas I. 2015. Mosquito records from Mexico: the mosquitoes (Diptera: Culicidae) of Tamaulipas State. Journal of Medical Entomology 52: 171184.

Peña A, Neyra L. 1998. Amenazas a la biodiversidad, pp. 157-182 In La diversidad biológica de México: estudio de país. Parte III. Manejo de los recursos naturales. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Mexico City, Distrito Federal, Mexico.

Pletsch DJ. 1986. A comparison of faunal list of mosquito species in Florida, in Cuba and in the state of Quintana Roo, Yucatan Peninsula, Mexico. Journal of the Florida Anti-Mosquito Association 57: 29-32.

Plyusnin A, Beaty BJ, Elliott RM, Goldbach R, Kormelink R, Lundkvist KA, Schmaljohn CS, Tesh RB. 2012. Family Bunyaviridae, pp. 725-741 In King AMQ, Ad-ams MJ, Carstens EB, Lefkowitz EJ [eds.], Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic, San Diego, California, USA.

Rodríguez H, De La Hoz F. 2005. Dengue and dengue and vector behaviour in Cáqueza, Colombia, 2004. Revista de Salud Pública 7: 1-15.

Rueda SJ, Hernández VR. 2008. Contribución al conocimiento de los culícidos del municipio de Torreblanca (Castellón, España) (Díptera: Culicidae). Boletín de la Asociación Española de Entomología 32: 315-325.

Talaga S, Leroy C, Céréghino R, Dejean A. 2016. Convergent evolution of intraguild predation in phytotelm-inhabiting mosquitoes. Evolutionary Ecology 30: 1133-1147.