Restricted accessResearch articleFirst published online 2022-02
Integrated Approaches for the Identification of Mosquitoes (Diptera: Culicidae) from the Volcanoes of Central America Physiographic Subprovince of the State of Chiapas,Mexico
Nowadays, there is a lack of information on the mosquito's fauna and DNA barcoding sequence reference library from many areas in Mexico, including the Volcanoes of Central America physiographic subprovince in the state of Chiapas. Consequently, a survey was undertaken to delineate the mosquito (Diptera: Culicidae) fauna in this region across different seasons using different collecting techniques. All species were identified by morphology and DNA barcoding, and their ecological features were also defined. In total, 62 taxa were morphologically examined, 60 of these were successfully identified based on morphological characteristics, but two were unable to be identified at the species level. The genera Aedes, Anopheles, Culex, and Wyeomyia are the most diverse among mosquito genera collected and include several species of medical and veterinary importance. Ecological characteristics of the immature habitats indicated that they were grouped into four categories namely, (1) large water bodies at ground level, (2) small and shady phytotelmata (e.g., tree holes and bamboo internodes), (3) large phytotelmata (e.g., plant leaves and axis bromeliad), and (4) artificial containers. The cytochrome c oxidase subunit I (COI) DNA barcoding sequences successfully separated the majority of these species, although specific species showed >2% intraspecific genetic divergences.
Get full access to this article
View all access options for this article.
References
1.
AdeniranAA, Hernández-TrianaLM, Ortega-MoralesAI, Garza-HernándezJA, et al.Identification of mosquitoes (Diptera: Culicidae) from Mexico State, Mexico using morphology and COI DNA barcoding. Acta Trop, 2020; 213:105730.
2.
AitkenTHG. Habits of some mosquito hosts of VEE (Mucambo) virus from northeastern South America, including Trinidad. In: Proceedings of the Workshop-Symposium on Venezuelan Encephalitis Virus. Washington D.C., September 1971. Pan American Health Organization,, 1972:254–256.
3.
AitkenTHG, AndersonCR. Virus transmission studies with Trinidadian mosquitoes. Am J Trop Med Hyg, 1959; 8:41–45.
4.
AitkenTHG, SpenceL, JonkersAH, AndersonCR. Wyeomyia-virus isolations in Trinidad, West Indies. Am J Trop Med Hyg, 1968; 17:886–888.
5.
AitkenTHG, SpenceL, JonkersAH, DownsWG. A 10-year survey of Trinidadian arthropods for natural virus infections (1953–1963). J Med Entomol, 1969; 6:207–215.
6.
AndersonCR, AitkenTHG, SpenceL, DownsWG. Kairi virus, a new virus from Trinidadian forest mosquitoes. Am J Trop Med Hyg, 1960; 9:70–72.
7.
AnisimovaM, GascuelO. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol, 2006; 55:539–552.
8.
AshfaqM, HebertPDN, MirzaJH, KhanAM, et al.Analyzing mosquito (Diptera: Culicidae) diversity in Pakistan by DNA barcoding. PLoS One, 2014; 9:e97268.
9.
AyersVB, HuangYJ, LyonsAC, ParkS, et al.Infection and transmission of Cache Valley virus by Aedes albopictus and Aedes aegypti mosquitoes. Parasit Vectors, 2019; 12:384.
10.
BarberMA, KompWHW, HayneTB. Malaria and malaria danger in certain irrigated regions of the southwestern United States. US Public Health Rep, 1929; 44:1300–1315.
11.
BarreraR, HunspergerE, Muñoz-JordánJL, AmadorA, et al.First isolation of West Nile virus in Caribbean. Am J Trop Med Hyg, 2008; 78:666–668.
12.
BarretoP, LeeVH. Artropodos hematofagos del rio Raposo, Valle, Colombia. II. Culicidae. Caldasia, 1969; 10:407–440.
13.
BeebeNW. DNA barcoding mosquitoes: Advice for potential prospectors. Parasitology, 2018; 145:622–633.
14.
BelkinJN, HeinemannSJ, PageWA. The culicidae of Jamaica (Mosquito studies. XXI). Contrib Am Entomol Inst, 1970; 1:1–451.
15.
BelkinJN, SchickRX, HeinemannSJ. Mosquito studies (Diptera, Culicidae) V. Mosquitoes originally described from Middle America. Contrib Am Entomol Inst, 1965; 1:1–95.
16.
Beltrán-AguilarA, Ibáñez-BernalS, Mendoza-PalmeroF, Sandoval-RuizCA, et al.Taxonomía y distribución de los Anofelinos en el estado de Veracruz, México (Diptera: Culicidae, Anophelinae). Acta Zool Mex, 2011; 27:601–755.
17.
BerlinOGW. Mosquito studies (Diptera, Culicidae) XII A revision of the Neotropical subgenus Howardina of Aedes. Contrib Am Entomol Inst, 1969; 4:1–189.
18.
BondJG, Casas-MartínezM, Quiroz-MartínezH, Novelo-GutiérrezR, et al.Diversity of mosquitoes and the aquatic insects associated with their oviposition sites along the Pacific coast of Mexico. Parasit Vectors, 2014; 7:1–19.
19.
BoydMF, KitchenSF, MulrennanJA. On the relative susceptibility of the inland and coastal varieties of An. crucians Wied. To P. falciparum Welch. Am J Trop Med, 1936; 16:159–161.
20.
BradyOJ, HaySI. The global expansión of dengue: How Aedes aegypti mosquitoes enabled the first pandemic arbovirus. Annu Rev Entomol, 2020; 65:191–208.
21.
BrocheroH, ParejaPX, OrtizG, OlanaVA. Sitios de cría y actividad de picadura de especies de Anopheles en el municipio de Cimitarra, Santander, Colombia. Biomedica, 2006; 26:269–277.
22.
BritoAC, FontesG, da RochaEMM, RochaDAM, et al.Development of Dirofilaria immitis (Leidy) in Aedes aegypti (L.) and Culex quinquefasciatus (Say) from Maceió, Alagoas. Mem Inst Oswaldo Cruz, 1999; 94:575–576.
23.
BurtonGJ. Attack on the vector of filariasisi in British Guiana. Public Health Rep, 1964; 79:137–143.
24.
CardosoBF, SerraOP, HeinenLB, ZuchiLB, et al.Detection of Oropuche virus segment S in patients and in Culex quinquefasciatus in the state of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz, 2015; 110:745–754.
25.
CardosoJd, de AlmeidaMA, dos SantosE, da FonsecaDF, et al.Yellow fever virus in Haemagogus leucocelaenus and Aedes serratus mosquitoes, southern Brazil, 2008. Emerg Infect Dis, 2010; 16:1918–1924.
26.
CarpenterSJ, LaCasseWJ. Mosquitoes of North America (North of Mexico). USA: University of California Press, 1955:1–495.
27.
Casas-MartínezM, BondJG, VillarealC, UlloaA. Vigilancia entomológica. In: Rodríguez MH, Ulloa A, Ramsey JM, eds. Manual Para la Vigilancia y el Control del Paludismo en Mesoamérica. México: Instituto Nacional de Salud Pública,, 2008:79–93.
28.
Casas-MartínezM, Orozco-BonillaA. Diversidad y distribución geográfica del género Anopheles en el sur de México. Biodiversitas, 2006; 67:12–15.
29.
Casas-MartínezM, Orozco-BonillaA, Muñoz-ReyesM, Ulloa-GarcíaA, et al.A new tent trap for monitoring the daily activity of Aedes aegypti and Aedes albopictus. J Vector Ecol, 2013; 38:277–288.
30.
CauseyOR, CauseyCE, MarojaOM, MacedoDG. The isolation of arthropod-borne viruses, including members of two hitherto undescribed serological groups in the Amazon region of Brazil. Am J Trop Hyg, 1961; 10:227–236.
31.
CDC: Centers for Disease Control and Prevention. Mosquito species in which West Nile virus has detected, United States, 199–2016 (reported to ArboNET). Available at https://www.cdc.gov/westnile/resources/pdfs/MosquitoSpecies1999-2016.pdf (Accessed December3, 2020).
32.
ChamberlainEW, KisslingEE, SikesEK. Studies on the North American arthropod-borne encephalitides. VII. Estimation of amount of Eastern equine encephalitis virus inoculated by infected Aedes aegypti. Am J Hyg, 1954; 60:286–291.
33.
ChanA, ChiangL, HapuarachchiHC, TanCH, et al.DNA barcoding: Complementing morphological identification of mosquito species in Singapore. Parasit Vectors, 2014; 7:569.
34.
Chan-ChableRJ, Martinez-ArceA, Mis-AvilaPC, Ortega-MoralesAI. Confirmation of occurrence of Anopheles (Anopheles) veruslanei Vargas in Quinatana Roo, Mexico using morphology and DNA barcodes. Acta Trop, 2018a; 188:138–141.
35.
Chan-ChableRJ, Martínez-ArceA, Mis-AvilaPC. Especies cripticas en Ochlerotatus taeniorhynchus mediante revelación de codigo de barras. Rev Salud Quintana Roo, 2018b; 11:7–11.
36.
Chan-ChableRJ, Martínez-ArceA, Mis-AvilaPC, Ortega-MoralesAI. DNA barcodes and evidence of cryptic diversity of anthropophagous mosquitoes in Quintana Roo, Mexico. Ecol Evol, 2019; 9:4692–4705.
37.
Chan-ChableRJ, Ortega-MoralesAI, Martínez-ArceA. First record of Psorophora albipes in Quintana Roo, Mexico. J Am Mosq Control Assoc, 2016; 32:237–239.
38.
ChaoA, ColwellRK, LinCW, GotelliNJ. Sufficient sampling for asymptotic minimum species richness estimators. Ecology, 2009; 90:1125–1133.
39.
Chouin-CarneiroT, Vega-RuaA, VazeilleM, YebakimaA, et al.Differential susceptibilities of Aedes aegypti and Aedes albopictus from the Americas to Zika virus. PLoS Negl Trop Dis, 2016; 10:e0004543.
40.
Clark-Gil, DarsieRF. The mosquitoes of Guatemala their identification, distribution and bionomics, with keys to adult females and larvae. Mosqu Syst, 1983; 15:151–284.
41.
CohenSB, LewoczkoK, HuddlestonDB, MoodyE, et al.Host feeding patterns of potencial vectors of Eastern equine encephalitis virus at an epizootic focus in Tenessee. Am J Trop Med Hyg, 2009; 81:452–456.
42.
CuppEW, HassanHK, YueX, OldlandWK, et al.West Nile virus infection in mosquitoes in the mid-south USA, 2002–2005. J Med Entomol, 2007; 44:117–125.
43.
CywinskaA, HunterFF, HebertPDN. Identifying Canadian mosquito species through DNA barcodes. Med Vet Entomol, 2006; 20:413–424.
44.
DarsieRF. A survey and bibliography of the mosquito fauna of Mexico (Diptera: Culicidae). J Am Mosq Control Assoc, 1996; 12:298–306.
45.
DeardorffER, Estrada-FrancoJG, FreierJE, Navarro-LopezR, et al.Candidate vectors and rodent hosts of Venezuelan equine encephalitis virus, Chiapas, 2006–2007. Am J Trop Med Hyg, 2011; 85:1146–1153.
46.
de Melo XimenesMFF, de Araújo GalvãoJM, InacioCLS, Macêdo E SilvaVP, et al.Arbovirus expansion: New species of culicids infected by the Chikungunya virus in an urban park of Brazil. Acta Trop, 2020; 209:105538.
47.
de Oliveira AragãoAO, Nunes NetoJP, CruzACR, CassebSMM, et al.Description and phylogeny of the mitochondrial genome of Sabethes chloropterus, Sabethes glaucodaemon and Sabethes belisarioi (Diptera: Culicidae). Genomics, 2019; 111:607–611.
48.
de RodanicheE, GalindoP. Isolation of yellow fever virus from Haemagogus mesodentatus, H. equinus and Sabethes chloropterus captured in Guatemala 1956. Am J Trop Hyg, 1957a; 6:232–237.
49.
de RodanicheE, GalindoP. Isolation of Ilhéus virus from Sabethes chloropterus captured in Guatemala in 1956. Am J Trop Hyg, 1957b; 6:686–687.
50.
de RodanicheE, GalindoP. Isolation of the virus of the Ilheus encephalitis form mosquitoes captured in Panama. Am J Trop Hyg, 1961; 10:393–394.
51.
de RodanicheE, GalindoP. Ecological observations of Ilheus virus in vicinity of Almirante, Republic of Panama. Am J Trop Hyg, 1963; 12:924–928.
52.
Demari-SilvaB, TavaresF, SallumMAM, ToledoM. Taxonomic and phylogenetic relationships between species of the genus Culex (Diptera: Culicidae) from Brazil inferred from the cytochrome c oxidase I mitochondrial gene. J Med Entomol, 2011; 48:272–279.
53.
DyarHG. The Mosquitoes of the Americas. Washington, D.C.: Carnegie Institution of Washington, 1928.
54.
DyarHG, KnabF. The larvae of culicidae as independent organisms. J N Y Entomol Soc, 1906; 14:169–230.
55.
Elizondo-QuirogaD, Medina-SánchezA, Sánchez-GonzálezJM, EckertKA, et al.Zika virus in salivary glands of five different species of wild-caught mosquitoes from Mexico. Sci Rep, 2017; 8:809.
56.
FaranME, LinthicumKJ. A handbook of the Amazonian species of Anopheles (Nyssorhynchus) (Diptera: Culicidae). Mosq Syst, 1981; 13:1–81.
57.
FillingerU, SombroekH, MajambereS, van LoonE, et al.Identifying the most productive breeding sites for malaria mosquitoes in The Gambia. Malar J, 2009; 8:1–14.
58.
FolmerO, BlackM, HoehW, LutzR, et al.DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol, 1994; 3:294–299.
59.
GalindoP, BlantonFS, PeytonEL. A revision of the Uranotaenia of Panama with notes on other American species of the genus (Diptera, Culicidae). Ann Entomol Soc Am, 1954; 47:107–177.
60.
GalindoP, PeraltaPH, MackenzieRB, BeyeHK. St. Louis encephalitis in Panama: A review and a progress report. Am J Trop Med Hyg, 1964; 13:455.
61.
GalindoP, SrihongseS. Transmission of arboviruses to hamsters by the bite of naturally infected Culex (Melanoconion) mosquitoes. Am J Trop Med Hyg, 1967; 16:525–530.
62.
GalindoP, SrihongseS, de RodanicheE, GraysonMA. An ecological survey for arboviruses in Almirante, Panama, 1959–1962. Am J Trop Med Hyg, 1966; 15:385–400.
63.
GómezGF, BickersmithSA, GonzálezR, ConnJE, et al.Molecular taxonomy provides new insights into Anopheles species of the Neotropical Arribalzagia series. PLoS One, 2015; 10:e0119488.
64.
González-CerónL, RodríguezMH, Nettel-CruzJA, Hernández-ÁvilaJE, et al.Plasmodium vivax CSP-Pvs25 variants from southern Mexico produce distinct patterns of infectivity for Anopheles albimanus versus An. pseudopunctipennis, in each case independent of geographical origin. Parasit Vectors, 2019; 12:86.
65.
GraysonMA, GalindoP. Epidemiologic studies of Venezuelan equine encephalitis virus in Almirante, Panama. Am J Epidemiol, 1968; 88:80–96.
66.
HarbachRE. Culicipedia: Species-Group, Genus-Group and Family-Group Names in Culicidae (Diptera). Boston: CABI, 2019:1–373.
67.
HarbachRE. Mosquito Taxonomic Inventory. Available at https://mosquito-taxonomic-inventory.info (Accessed April7, 2020).
68.
HebertPDN, CywinskaA, BallSL, deWaardJR. Biological identifications through DNA barcodes. Proc R Soc Biol Sci, 2003a; 270:313–321.
69.
HebertPDN, RatnasinghamS, deWaardJR. Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Biol Sci, 2003b; 270:S96–S99.
70.
Hernández-TrianaLM, BrugmanVA, NikolovaNI, Ruiz-ArrondoI, et al.DNA barcoding of British mosquitoes (Diptera, Culicidae) to support species identification, discovery of cryptic genetic diversity and monitoring invasive species. ZooKeys, 2019; 832:57–76.
71.
Hernández-TrianaLM, BrugmanVA, ProsserSWJ, WelanC, et al.Molecular approaches for blood meal analysis and species identification of mosquitoes (Insecta: Diptera: Culicidae) in rural locations in southern England, United Kingdom. Zootaxa, 2017; 4250:67–76.
72.
Hernández-TrianaLM, Garza HernándezJA, Ortega MoralesAI, ProsserSWJ. An integrated molecular approach to untangling host-vector-pathogen interactions in mosquitoes (Diptera: Culicidae) from sylvan communities in Mexico. Front Vet Sci, 2021; 7:564791.
73.
Hoyos-LópezR, Suaza-VascoJ, Rúa-UribeG, UribeS, et al.Molecular detection of flaviviruses and alphaviruses in mosquitoes (Diptera: Culicidae) from coastal ecosystems in the Colombian Caribbean. Mem Inst Oswaldo Cruz, 2016; 111:625–634.
74.
INE: Instituto Nacional de Ecología. Insumos Para el Ordenamiento Ecológico de la Zona Trópico Húmedo. México: Mapas y gráficos S.A. de C.V.,, 1989:1–47.
75.
INEGI: Instituto Nacional de Estadística y Geografía. Uso de suelo y vegetación. 2019. Available at https://www.inegi.org.mx/temas/usosuelo
76.
JonesJW, TurellMJ, SardelisMR, WattsDM, et al.Seasonal distribution, biology, and human attraction patterns of Culicine mosquitoes (Diptera: Culicidae) in a Forest near Puerto Almendras, Iquitos, Peru. J Med Entomol, 2004; 41:349–360.
77.
JuddDD. Review of the systematics and phylogenetic relationships of the Sabethini (Diptera: Culicidae). Syst Entomol, 1996; 21:129–150.
78.
KamgangB, VazeilleM, YougangAP, TedjouAN, et al.Potential of Aedes albopictus and Aedes aegypti (Diptera: Culicidae) to transmit yellow fever virus in urban areas in Central Africa. Emerg Microbes Infect, 2019; 8:1636–1641.
79.
KasaiN, WilliamP. Infecção experimental de Aedes fluviatilis (Lutz, 1904) por Dirofilaria immitis (Leidy, 1856). Rev Brasil Biol, 1986; 46:277–283.
80.
KisslingRE. The arthropod-borne viruses of man and other animals. Annu Rev Microbiol, 1960; 14:261–282.
81.
KumarS, StecherG, LiM, KnyazC, et al.MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol, 2018; 35:1547–1549.
82.
LabartheN, SerranoML, MeloYF, de OliveiraSJ, et al.Mosquito frequency and feeding habits in an exotic canine dirofilariasis area of Niteroi, state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz, 1998; 93:145–154.
83.
LaneJ. Neotropical Culicidae. Vol. II. Brazil: University of São Paulo, Brazil, 1953:553–1099.
84.
LaneJ, CerqueiraNL. Os Sabetineos da America (Diptera, Culicidae). Arqu Zool, 1942; 9:473–692.
85.
LauritoM, AlmirónW. Phylogenetic relationship of Culex (Culex) species (Diptera, Culicidae) from Argentina based on morphological characters. Zootaxa, 2013; 3652:117–155.
86.
LauritoM, AyalaAM, AlmirónWR, GardenalCN. Molecular identification of two Culex (Culex) species of the neotropical region (Diptera: Culicidae). PLoS One, 2017; 12:e0173052.
87.
LauritoM, OliveiraTMP, AlmirónWR, SallumMAM. COI barcode versus morphological identification of Culex (Culex) (Diptera: Culicidae) species: A case study using samples from Argentina and Brazil. Mem I Oswaldo Cruz, 2013; 108:110–122.
LongKC, ZieglerSA, ThangamaniS, HausserNL, et al.Experimental transmission of Mayaro virus by Aedes aegypti. Am J Trop Med Hyg, 2011; 85:750–757.
90.
LutomiahJJL, MwandawiroC, MagamboJ, SangRC. Infection and vertical transmission of Kamiti river virus in laboratory bred Aedes aegypti mosquitoes. J Insect Sci, 2007; 7:1–7.
91.
Manrique-SaideP, Escobedo-OrtegónJ, Bolio-GonzálezM, Sauri-ArceoC, et al.Incrimination of the mosquito, Aedes taeniorhynchus as the primary vector of heartworm, Dirofilaria immitis, in coastal Yucatan, México. Med Vet Entomol, 2010; 24:456–460.
92.
MarchiMJ, PereiraPA, de MenesesRM, TubakiRM. New records of mosquitoes carrying Dermatobia hominis eggs in the state of São Paulo, southeastern Brazil. J Am Mosq Control Assoc, 2012; 28:116–118.
93.
Martínez-PalaciosA. Nota sobre la distribución de los mosquitos Culex en México (Diptera, Culicidae). Rev Soc Mex Hist Nat, 1952; 13:75–87.
94.
MartiniE. Los mosquitos de México. Boletines Técnicos Departamento de Salubridad Pública serie A: Entomología Médica y Parasitología, 1935; 1:1–66.
95.
MitchellCJ. Vector competence of North and South American strains of Aedes albopictus for certain arboviruses: A review. J Am Mosq Control Assoc, 1991; 7:446–451.
96.
MitchellCJ, MorrisCD, SmithGC, KarabastosN, et al.Arboviruses associated with mosquitoes from nine Florida counties during 1993. J Am Mosq Control Assoc, 1996; 12:255–262.
97.
MitchellCJ, NiebylskiML, SmithGC, KarabatsosN, et al.Isolation of Eastern equine encephalitis virus from Aedes albopictus in Florida. Science, 1992; 257:526–527.
98.
Montero-PauJ, GómezA, MuñozJ. Application of an inexpensive and high-throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnol Oceanogr Meth, 2008; 6:218–222.
NasciRS, MitchellCJ. Larval diet, adult size, and susceptibility of Aedes aegypti (Diptera: Culicidae) to infection with Ross river virus. J Med Entomol, 1994; 31:123–126.
101.
NavarroJC, LiriaJ, PiñangoH, BarreraR. Biogeographic area relationships in Venezuela: A parsimony analysis of Culicidae-Phytotelmata distribution in national parks. Zootaxa, 2007; 1547:1–20.
102.
OlanoVA, CarrilloMP, EspinalCA. Estudios de infectividad de la especie Anopheles albimanus Wiedemann, 1820 (Diptera: Culicidae) cepa Cartagena, con plasmodios humanos. Biomedica, 1985; 5:5–10.
103.
Ortega-MoralesA, ZavortinkT, Huerta-JiménezH, Ibáñez-BernalS. The mosquitoes (Diptera: Culicidae) of Hidalgo state, Mexico. Acta Trop, 2019; 189:94–103.
104.
OrtizDI, KangW, WeaverSC. Susceptibility of Ae. aegypti (Diptera: Culicidae) to infection with epidemic (subtype IC) and enzootic (subtypes ID, IIIC, IIID) Venezuelan equine encephalitis complex alphaviruses. J Med Entomol, 2008; 45:1117–1125.
105.
PadialJM, MirallesA, De la RivaI, VencesM. The integrative future of taxonomy. Front Zool, 2010; 7:1–14.
106.
PecorJE, HarbachRE, PeytonEL, RobertsDR, et al.Mosquitoes studies in Belize, Central America: Records, taxonomic notes, and a checklist of species. J Am Mosq Control Assoc, 2002; 18:241–276.
107.
PeñaA, KummHW. Algunas consideraciones generals sobre la miasis cutanea (tórsalo) en Costa Rica. Rev Med, 1939; 64:635–641.
108.
Pereira-SilvaJW, Ríos-VelásquezCM, LimaGRd, Marialva dos SantosEF, et al.Distribution and diversity of mosquitoes and Oropuche-like virus infection rates in an Amazonian rural settlement. PLoS One, 2021; 16:e0246932.
109.
PothikasikornJ, BangsMJ, BoonplueangR, ChareonviriyaphapT. Susceptibility of various mosquitoes of Thailand to nocturnal subperiodic Wuchereria bancrofti. J Vector Ecol, 2008; 33:313–320.
110.
PuggioliA, BonilauriP, CalzolariM, LelliD, et al.Does Aedes albopictus (Diptera: Culicidae) play any role in Usutu virus transmission in Northern Italy? Experimental oral infection and field evidences. Acta Trop, 2017; 172:192–196.
111.
RatnasinghamS, HebertPDN. A DNA-Based Registry for all animal species: The Barcode Index Number (BIN) System. PLoS One, 2013; 8:e66213.
112.
Rosero-GarcíaD, Rúa-UribeG, CorreaMM, ConnJE, et al.Mosquito (Diptera: Culicidae) grouping based on larval habitat characteristics in high mountain ecosystems of Antioquia, Colombia. J Vector Ecol, 2018; 43:71–79.
113.
RuedaLM. Global diversity of mosquitoes (Insecta: Diptera: Culicidae) in freshwater. In: BalianEV, LévêqueC, SegersH, MartensK, eds. Freshwater Animal Diversity Assessment. Developments in Hydrobiology. Dordrecht, Netherlands: Springer, 2008:477–487.
114.
SallumMA, ForattiniOP. Revision of the Spissipes section of Culex (Melanoconion) (Diptera: Culicidae). J Am Control Assoc, 1996; 12:517–600.
115.
SanmartínC, MackenzieRB, TrapidoH, BarretoP, et al.Encefalitis equina venezolana en Colombia, 1967. Bol Sanit Panam, 1973; 74:108–137.
116.
SchererWF, DickermanRW, Diaz-NajeraA, WardBA, et al.Ecologic studies of Venezuelan encephalitis virus in southeastern México. 3. Infection of mosquitoes. Am J Trop Med Hyg, 1971; 20:969–979.
117.
SchickRX. Mosquito studies (Diptera, Culicidae) XX The Terrens group of Aedes (Finlaya). Contrib Am Entomol Inst, 1970; 5:1–157.
118.
SellersRF, BergoldGH, SuárezOM, MoralesA. Investigations during Venezuelan equine encephalitis outbreaks in Venezuela—1962–1964. Am J Trop Med Hyg, 1965; 14:460–469.
119.
SEMARNAT. Secretaria de medio ambiente y recursos naturales. Programa de manejo reserva de la biosfera Volcán Tacaná. México; SEMARNAT/CONANP,, 2013:1–299.
120.
ShamanJ, DayJF, StieglitzM. Drought-induced amplification of Saint Louis encephalitis virus, Florida. Emerg Infect Dis, 2002; 8:575–580.
121.
SilverJB. Mosquito Ecology Field Sampling Methods. New York: Springer, 2008:1–1477.
122.
SirivanakarnS. A review of the systematics and a proposed scheme of internal classification of the new world subgenus Melanoconion of Culex (Diptera, Culicidae). Mosq Syst, 1982; 14:265–333.
123.
SoperFL, PennaH, CardosoE, SerafimJJR, et al.Yellow fever without Aedes aegypti. Study of a rural epidemic in the Valle do Chanaan, Espirito Santo, Brazil, 1932. Am J Epidemiol, 1933; 18:555–587
124.
SpenceL, AndersonCR, AitkenTHG, DownsWG. Aruac virus, a new agent isolated from Trinidadian mosquitoes. Am J Trop Med Hyg, 1966; 15:231–234.
125.
Spence BeaulieuMR, FedericoJL, ReiskindMH. Mosquito diversity and dog heartworm prevalence in suburban areas. Parasit Vectors, 2020; 13:1–12.
126.
StoneA. Breding-Archbold-Smithsonian biological survey of Dominica: The mosquitoes of Dominica (Diptera: Culicidae). P Entomol Soc Wash, 1969; 70:384.
127.
SudiaWD, LordRD, NewhouseVF, MillerDL, et al.Vector host-studies of an epizootic of Venezuelan equine encephalomyelitis in Guatemala, 1969. Am J Epidem, 1971; 93:137–143.
128.
TalagaS, LeroyC, GuidezA, DusfourI, et al.DNA reference libraries of French Guianese mosquitoes for barcoding and metabarcoding. PLoS One, 2017; 12:e0176993.
129.
TriteeraprapabS, KanjanopasK, SuwannadabbaS, SangprakarnS, et al.Transmission of the nocturnal periodic strain of Wuchereria bancrofti by Culex quinquefasciatus: Stablishing the potential for urban filariasis in Thailand. Epidemiol infect, 2000; 125:207–212.
130.
TurellMJ. Members of the Culex pipiens complex as vectors of viruses. J Am Mosq Control Assoc, 2012; 28:123–126.
131.
TurellMJ, BritchSC, AldridgeRL, KlineDL, et al.Potential for mosquitoes (Diptera: Culicidae) from Florida transmit Rift Valley fever virus. J Med Entomol, 2013; 50:1111–1117.
132.
TurellMJ, O'GuinnML, DohmDJ, JonesJW. Vector competence of North American mosquitoes (Diptera: Culicidae) for West Nile virus. J Med Entomol, 2001; 38:130–134.
133.
UlloaA, FergusonHH, Méndez-SánchezJD, Danis-LozanoR, et al.West Nile virus activity in mosquitoes and domestic animals in Chiapas, Mexico. Vector Borne Zoonotic Dis, 2009; 9:555–560.
134.
UnluI, KramerWL, RoyAF, FoilLD. Detection of West Nile virus RNA mosquitoes and identification of mosquito blood meals collected at alligator farms in Louisiana. J Med Entomol, 2010; 47:625–633.
135.
ValenciaJD. Mosquito studies (Diptera, Culicidae) XXXI A revision of the subgenus Carrollia of Culex. Contrib Am Entomol Inst, 1973; 9:1–133.
136.
VasconcelosPF, Travassos da RosaJFS, Travassos da RosaAPA, DégallierN. Epidemiologia das encefalites por arbovírus na Amazônia brasileira. Rev Inst Med trop São Paulo, 1991; 33:465–476.
137.
Vega-RúaA, ZouacheK, GirodR, FaillouxAB, et al.High level of vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor in the spread of Chikungunya virus. J Virol, 2014; 88:6294–6306.
138.
VersteirtV, NagyZT, RoelantsP, DenisL, et al.Identification Belgian mosquito species (Diptera: Culicidae) by DNA barcoding. Mol Ecol Resour, 2014; 15:449–457.
139.
VillalobosG. El contexto físico y su importancia para la preservación de la biodiversidad. In: CruzA, MelgarejoED, CamachoF, NájeraKC, eds. La biodiversidad en Chiapas: Estudio de estado. Comisión nacional para el conocimiento y uso de la biodiversidad. Gobierno del estado de Chiapas México: CONABIO, 2013:27–40.
140.
Walter Reed Biosystematics Unit (WRBU). Johnbelkinia genus page 2021a. Walter Reed Biosystematics Unit Website, Available at http://wrbu.si.edu/vectorspecies/genera/johnbelkinia (Accessed July19, 2021).
141.
Walter Reed Biosystematics Unit (WRBU). Sabethes chloropterus species page 2021b. Walter Reed Biosystematics Unit Website. Available at http://wrbu.si.edu/vectorspecies/mosquitoes/chloropterus (Accessed July19, 2021).
142.
WangG, LiC, GuoX, XingD, et al.Identifying the main mosquitoes species in China based on DNA barcoding. PLoS One, 2012a; 7:e47051.
143.
WangZ, ZhangX, LiC, ZhangY, et al.Vector competence of five common mosquito species in the People´s Republic of China for Western equine encephalitis virus. Vector Borne Zoonotic Dis, 2012b; 12:605–608.
144.
WilkersonRC, StrickmanD, Fernández-SalasI, Ibáñez-BernalS. Clave ilustrada para la identificación de las hembras de mosquitos anofelínos de México y Centroamérica. México: Secretaria de Salud,, 1996:46.
145.
YangGJ, BrookBW, WhelanPI, ClelandS, et al.Endogenous and exogenous factors controlling temporal abundance patterns of tropical mosquitoes. Ecol Appl, 2008; 18:2028–2040.
146.
ZavortinkTJ. Mosquito studies (Diptera, Culicidae) XXVIII The new world species formerly placed in Aedes (Finlaya). Contrib Am Entomol Inst, 1972; 8:1–205.
147.
ZavortinkTJ. Mosquito studies (Diptera, Culicidae) XXXV The new sabethine genus Johnbelkinia and a preliminary reclassification of the composite genus Trichoprosopon. Contrib Am Entomol Inst, 1979; 17:1–60.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
