ABSTRACT

Collections of mosquitoes were conducted as part of the entomological vector surveillance in Quintana Roo State, Mexico, during September 2015. Species collected included Anopheles gabaldoni, An. darlingi, Psorophora columbiae, Culex inflictus, Cx. trifidus, Cx. lactator, and Wyeomyia guatemala s.l. All the specimens were identified by morphological and molecular characters (DNA-barcoding). This is the 1st time these species are reported in the Mexican state of Quintana Roo. This research updates and increases the list of species of mosquitoes in Quintana Roo from 79 to 86.

Culicidae is the most important group of insects worldwide from a medical and veterinary point of view; some species are vectors of pathogens that cause diseases which affect humans and domestic animals (Meisch 1994). Pathogens, like arboviruses, cause diseases such as dengue, Zika, chikungunya, yellow fever, West Nile virus, Mayaro fever, and Venezuelan equine encephalitis (Díaz-González et al. 2015). In tropical countries, diseases caused by mosquitoes are a priority in talking about health problems (Campos et al. 2017). In Quintana Roo State the last 4 years, the Secretary of State for Health has reported an average of 700 cases of patients with a mosquito-borne disease, including malaria, dengue, chikungunya, and Zika (DGE 2019). Consequently, knowledge about the distribution of the species with medical importance across the different states in Mexico has been useful for the public health authorities, in order to establish the relevant control strategies. Based on morphological and molecular evidence (DNA-barcoding), in Quintana Roo State are reported 7 new records: Anopheles (Anopheles) gabaldoni Vargas, An. (Nyssorhynchus) darlingi Root, Psorophora (Grabhamia) columbiae (Dyar and Knab), Culex (Culex) inflictus Theobald, Cx. (Melanoconion) trifidus (Dyar), Cx. (Phenacomyia) lactator Dyar and Knab, and Wyeomyia (Wyeomyia) guatemala (Dyar and Knab) s.l. for the 1st time. In this research, the list of species that are distributed in the state of Quintana Roo has been updated (Table 1).

Table 1.

Updated checklist of mosquito species of the Quintana Roo State.

Updated checklist of mosquito species of the Quintana Roo State.
Updated checklist of mosquito species of the Quintana Roo State.

In September 2015, 324 adult female mosquitoes were collected, using the Centers for Disease Control and Prevention (CDC) light traps that operated consecutively from 5:00 p.m. to 10:00 p.m. The traps were installed near the international border between Mexico and Belize in 3 locations (2 traps per location): Sacxan (18°27′52.76″N, 88°30′58.44″W; 18°27′44.61″N, 88°31′08.44″W), Palmar (18°26′43.0″N, 88°31′27.4″W; 18°26′26.9″N, 88°31′37.99″W), and Ramonal (18°25′27.7″N, 88°31′45.97″W; 18°25′08.1″N, 88°31′47.7″W). All traps were baited with CO2 and hung at 40 cm above ground level. Additionally, mosquitoes were collected using manual aspirators while the collecting personnel were approaching. All specimens collected were deposited in the Entomology Collection of the Zoology Museum of El Colegio de la Frontera Sur, Chetumal Unit, with reference code ECO-CH-AR/DP_0285-0611.

A stereomicroscope (Discovery V8; Zeiss, Jena, Germany) and identification keys of Clark-Gil and Darsie (1983) and Wilkerson and Strickman (1990) were used for taxonomic identification. For molecular analysis, DNA-barcoding region cytochrome c oxidase I was used. All selected specimens (n = 18) (Table 2) were processed according to previously reported protocols (Chan-Chable et al. 2019b). The 18 sequences obtained here were deposited in the BOLD Systems database (Ratnasingham and Hebert 2007) within the project “New Records of Culicids from Ribera del Rio Hondo Chetumal, Mexico” (Project code: NRC). Molecular analysis confirms the identification of species and this study corresponds to the 7 new records (Table 2). The sequences of An. gabaldoni and Cx. inflictus are new to the GenBank database. Meanwhile, the sequences of Cx. trifidus have the Barcode Index Number: BOLD: ADE4670. This number was new for GenBank and BOLD Systems databases (Table 2).

Table 2.

Sampling locality of the species collected and processed in this study, number of sequences analyzed, and Barcode Index Number codes (BINs) assigned by BOLD Systems.

Sampling locality of the species collected and processed in this study, number of sequences analyzed, and Barcode Index Number codes (BINs) assigned by BOLD Systems.
Sampling locality of the species collected and processed in this study, number of sequences analyzed, and Barcode Index Number codes (BINs) assigned by BOLD Systems.

Anopheles gabaldoni is reported in Guatemala, Belize, and southern Mexico (WRBU 2005). In Mexico, it had been previously recorded in the states of Veracruz, Tabasco, Chiapas, and Campeche (Vargas and Martínez-Palacios 1956, Ordóñez-Sánchez et al. 2013). In this study 6 adult females were collected: 2 specimens were from Sacxan and 4 from Ramonal.

Anopheles darlingi is distributed from some states of southern Mexico to northern Argentina, through the chain of the Andes and the coast of the Atlantic Ocean in South America (Hiwat and Bretas 2011). In Mexico, An. darlingi had been previously recorded in Chiapas, Tabasco, and Campeche (Kumm et al. 1943, Vargas and Martínez-Palacios 1956). Anopheles darlingi is considered the main vector of malaria in the Neotropical region by its susceptibility to Plasmodium species and its anthropophilic behavior (Hiwat and Bretas 2011, Campos et al. 2017). In this study, 2 adult specimens were collected at 2100 h, 10 m from the Río Hondo in Ramonal locality.

Psorophora columbiae has been reported in the Bahamas, Belize, Canada, the Cayman Islands, Cuba, Mexico, and the USA (Meisch 1994). The distribution of Ps. columbiae in Mexico includes the states of Campeche, Chiapas, Coahuila, Durango, Morelos, Nuevo Leon, San Luis Potosi, Sonora, Tabasco, Tamaulipas, Veracruz, and Yucatán (Martini 1935, Vargas 1956, Díaz-Nájera and Vargas 1973, Heinemann and Belkin 1977). Furthermore, this revision also shows a female of Ps. columbiae that was collected in CDC trap at 1800 h in Sacxan locality.

Culex inflictus has also been distributed in the Antilles, Barbados, Belize, Colombia, Costa Rica, Cuba, Dominica, El Salvador, Grenada, Guatemala, Honduras, Martinique, Mexico, Nicaragua, Panama, Trinidad and Tobago, and Venezuela (WRBU 2005). In Mexico, Cx. inflictus has been recorded in Colima, Veracruz, Jalisco, Guerrero, and Chiapas (Martínez-Palacios 1952, Díaz-Nájera and Vargas 1973, Heinemann and Belkin 1977). Culex inflictus is a coastal species whose larvae develop in water in crab holes. The immature stages are commonly associated with Deinocerites cancer Theobald and De. epitedeus (Knab) (Martínez-Palacios 1952). The medical importance of Cx. inflictus is unknown. In this study, 2 females within a CDC trap were collected at 2100 h in Ramonal locality.

Culex trifidus has been scattered in Costa Rica, El Salvador, Guatemala, Honduras, Mexico, and Panama (WRBU 2005). In Mexico, Cx. trifidus has been recorded in the states of Guerrero, Michoacan, Morelos (Díaz-Nájera and Vargas 1973), Oaxaca (Heinemann and Belkin 1977), and in this study reported from Quintana Roo. The immature stages of Cx. trifidus develop in small bodies of water on the banks of rivers, as well as bodies of permanent water, with partial shade. Regularly, Cx. trifidus is associated with larvae of An. argyritarsis (Robineau-Desvoidy) and Cx. coronator (Dyar and Knab) (Heinemann and Belkin 1977, Clark-Gil and Darsie 1983). The medical importance of Cx. trifidus is unknown. Furthermore, this investigation displays that 310 females were collected in the 3 different localities (Table 2). All specimens were collected around 1800 and 2200 h at the located sites between 20 and 50 m from the Río Hondo.

Culex lactator has been dispersed in Belize, Colombia, Guatemala, Honduras, Mexico, Panama, and Venezuela (WRBU 2005). In Mexico, Cx. lactator has been recorded in the states of Chiapas, Hidalgo, Oaxaca, Tamaulipas, Veracruz, and Yucatan (Strickman and Pratt 1989, Ibáñez-Bernal and Martínez-Campos 1994, Zapata-Peniche et al. 2007, Ortega-Morales et al. 2015). In this investigation, an adult female was collected at 2000 h in Palmar.

Wyeomyia guatemala s.l. has been spread in Costa Rica, Guatemala, and Mexico (WRBU 2005). In Mexico, Wy. guatemala s.l. has been collected in the states of Chiapas, San Luis Potosí, Oaxaca, Tabasco, and Veracruz (Vargas 1956, Díaz-Nájera and Vargas 1973). Females have been collected in jungle areas and their larvae have been found in bromeliad axils (Vargas 1956). Likewise, 2 adult females were collected at 1600 h, resting on the collection personnel in the Sacxan and Ramonal localities, 20 m from the Río Hondo.

In Belize, the adjacent country, 112 mosquito species have been recorded (Pecor et al. 2002, Ortega-Morales et al. 2010b), of which 53 have not yet been recorded in Quintana Roo. Considering that the Quintana Roo State has a bigger area than Belize, 50,212 km2 versus 22,800 km2, respectively, and both regions bear similar environmental (urban, suburban, and wild) and climate conditions, it is predicted that there are still missing species to be recorded in Quintana Roo. The aforementioned highlights the necessity to increase the entomological studies of systematic collections, including stages of immature and adult mosquitoes from different biogeographic subregions, with different environments and different types of habitats.

We thank Edgardo Baalam, Gemma Macías, Irving Ramírez, and Nancy Cupul for the support during data collection trips. Our gratitude to Noemi Salas for the laboratory support, the Consejo Nacional de Ciencia y Tecnología (CONACYT) Mexico for the PhD scholarship provided to Rahuel J. Chan-Chable, and the Red MEXBOL project no. 271108 for funding.

REFERENCES CITED

REFERENCES CITED
Campos
M,
Conn
JE,
Peres-Alonso
D,
Vinetz
JM,
Emerson
KJ,
Martins Ribolla
PE
.
2017
.
Microgeographical structure in the major Neotropical malaria vector Anopheles darlingi using microsatellites and SNP markers
.
Parasit Vectors
10:76.
Chan-Chable
RJ,
Bahena-Basave
H,
Vázquez-Marroquín
R.
2019
a.
Nuevo registro de distribución para Trichoprosopon digitatum (Rondani) (Diptera: Culicidae) en Quintana Roo, México
.
Rev Chil Entomol
45
:
669
672
.
Chan-Chable
RJ,
Martínez-Arce
A,
Mis-Ávila
PC,
Ortega-Morales
AI.
2019
b.
DNA barcodes and evidence of cryptic diversity of anthropophagous mosquitoes in Quintana Roo, Mexico
.
Ecol Evol
9
:
4692
4705
.
Chan-Chable
RJ,
Ortega-Morales
AI,
Martínez-Arce
A.
2016
.
First record of Psorophora albipes in Quintana Roo, Mexico
.
J Am Mosq Control Assoc
32
:
237
240
.
Clark-Gil
S,
Darsie
RF.
1983
.
The mosquitoes of Guatemala, their identification, distribution and bionomics
.
Mosq Syst
15
:
151
284
.
DGE [Direccion General de Epidemiología].
2019
.
Boletín Epidemiológico, Sistema Nacional de Vigilancia Epidemiológica, Sistema Único de Información
[Internet].
México DF, México: Direccion General de Epidemiología
Diáz-González
EE,
Kautz
TF,
Dorantes-Delgado
A,
Malo-García
IR,
Laguna-Aguilar
M,
Langsjoen
RM,
Chen
R,
Auguste
DI,
Sanchéz-Casas
RM,
Danis-Lozano
R,
Weaver
SC,
Fernández-Salas
I.
2015
.
First report of Aedes aegypti transmission of chikungunya virus in the Americas
.
Am J Trop Med Hyg
93
:
1325
1329
.
Díaz-Nájera
A,
Vargas
L.
1973
.
Mosquitos mexicanos, distribución geográfica actualizada
.
Rev Invest Salud Pública
33
:
111
125
.
Heinemann
SJ,
Belkin
JN.
1977
.
Collection records of the project “Mosquitoes of Middle America” 9. Mexico (MEX, MF, MT, MX)
.
Mosq Syst
9
:
483
535
.
Hiwat
H,
Bretas
G.
2011
.
Ecology of Anopheles darlingi Root with respect to vector importance: a review
.
Parasit Vectors
4:177.
Ibáñez-Bernal
S,
Canul
O,
Camal
JF.
1990
.
Los dípteros de la reserva de la biosfera de Sian Ka'an, Quintana Roo, México
.
In:
Diversidad biológica de Sian ka'an, Quintana Roo, México
.
Gainesville, FL
:
Centro de Investigaciones de Quintana Roo y Program for Studies in Tropical Conservation, Univ. of Florida
.
p
305
316
.
Ibáñez-Bernal
S,
Martínez-Campos
C.
1994
.
Clave para la identificación de las larvas de mosquitos comunes en las áreas urbanas y suburbanas de la República Mexicana (Diptera: Culicidae)
.
Folia Entomol Mex
92
:
43
73
.
Kumm
HW,
Bustamante
ME,
Herrera
JR.
1943
.
Informe sobre algunos Anopheles hallados en la frontera de Mexico y Guatemala
.
Rev Inst Salub Enferm Trop
4
:
183
187
.
Martínez-Palacios
A.
1952
.
Culex inflictus Theobald y Culex thriambus Dyar, mosquitos nuevos para Mexico (Diptera: Culicidae)
.
Rev Soc Mex Hist Nat
13
:
89
95
.
Martini
E.
1935
.
Los mosquitos de México. Boletines Técnicos 1
.
México D.F., México
:
Departamento de Salubridad Pública
.
66
p.
Meisch
MV.
1994
.
The dark ricefield mosquito Psorophora columbiae
.
Wing Beats
5
:
8
9
.
Mis Ávila
PC,
'
Canul Amaro
GJ,
Domínguez Galera
MA.
2013
.
Taxonomic determination of mosquitoes (Culicinae: Culicidae) from the urban area of Chetumal, Quintana Roo
.
Rev Salud QRoo
6
:
8
13
.
Ordóñez-Sánchez
F,
Sánchez-Trinidad
A,
Mis-Ávila
PC,
Canul-Amaro
G,
Fernández-Salas
I,
Ortega-Morales
AI.
2013
.
Nuevos registros de mosquitos (Diptera: Culicidae) en algunas localidades de Campeche y Quintana Roo
.
Entomol Mex
1
:
850
854
.
Ortega-Morales
AI,
Casas-Martínez
M,
Bond
JG,
Harbach
RE.
2018
.
First records of Psorophora cilipes and Culex theobaldi in Quintana Roo State, Mexico
.
J Am Mosq Control Assoc
34
:
124
127
.
Ortega-Morales
AI,
Mis Ávila
P,
Elizondo-Quiroga
A,
Harbach
RE,
Siller-Rodríguez
QK,
Fernández-Salas
I
.
2010
a.
The mosquitoes of Quintana Roo State, Mexico (Diptera: Culicidae)
.
Acta Zool Mex (n.s.)
26
:
33
46
.
Ortega-Morales
AI,
Mis-Ávila
P,
Domínguez-Galera
M,
Canul-Amaro
G,
Esparza-Aguilar
J,
Carlos-Azueta
J,
Fernández-Salas
I.
2010
b.
First record of Stegomyia albopicta [Aedes albopictus] in Belize
.
Southwest Entomol
35
:
197
199
.
Ortega-Morales
AI,
Zavortink
TJ,
Huerta-Jiménez
H,
Sánchez-Ramos
FJ,
Valdéz-Pérezgasca
T,
Reyes-Villanueva
F,
Siller-Rodríguez
QK,
Fernández-Salas
I.
2015
.
Mosquito records from Mexico: the mosquitoes (Diptera: Culicidae) of Tamaulipas State
.
J Med Entomol
52
:
171
184
.
Pecor
JE,
Harbach
RE,
Peyton
EL,
Roberts
DR,
Rejmankova
E,
Manguin
S,
Palanko
J.
2002
.
Mosquito studies in Belize, Central America: records, taxonomic notes, and a checklist of species
.
J Am Mosq Control Assoc
18
:
241
276
.
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
.
J Fla Anti-Mosq Assoc
57
:
29
32
.
Ratnasingham
S,
Hebert
PDN.
2007
.
BOLD: the Barcode of Life Data System (http://www.barcodinglife.org)
.
Mol Ecol Notes
7
:
355
364
.
Salomón-Grajales
J,
Lugo-Moguel
GV,
Tinal-Gordillo
VR,
de La Cruz-Velazquez
J,
Beaty
BJ,
Eisen
L,
Lozano-Fuentes
S,
Moore
CG,
Garcia-Rejon
JE.
2012
.
Aedes albopictus mosquitoes, Yucatan Peninsula, Mexico
.
Emerg Infect Dis
18
:
525
527
.
Strickman
D,
Pratt
J.
1989
.
Redescription of Cx. corniger Theobald and elevation of Culex (Culex) lactator Dyar and Knab from synonymy based on specimens from Central America (Diptera: Culicidae)
.
Proc Entomol Soc Wash
91
:
551
574
.
Vargas
DL.
1956
.
Especies y distribución de mosquitos mexicanos no Anofelinos (Insecta, Diptera)
.
Rev Inst Salub Enf Trop
16
:
19
36
.
Vargas
DL.
1958
.
Nuevos datos sobre la distribución de anofelinos mexicanos
.
Bol Epidemiol
22
:
33
45
.
Vargas
DL.
1979
.
Anopheles (Anopheles) veruslanei Vargas, n. sp. (Diptera: Culicidae)
.
Gaceta Méd Méx
115
:
87
88
.
Vargas
L,
Martínez-Palacios
A.
1950
.
Estudio taxonómico de los mosquitos Anofelinos de México
.
México DF, México
:
Secretaría de Salubridad y Asistencia
.
Vargas
L,
Martínez-Palacios
A.
1956
.
Anofelinos mexicanos. Taxonomía y distribución
.
México DF, México
:
Secretaría de Salubridad y Asistencia, Comisión Nacional para la Erradicación del Paludismo
.
Wilkerson
RC,
Strickman
D.
1990
.
Illustrated key to the female Anopheline mosquitoes of Central America and Mexico
.
J Am Mosq Control Assoc
6
:
7
34
.
WRBU [Walter Reed Biosystematics Unit].
2005
.
Systematic catalog of Culicidae
[Internet].
Suitland, MD
:
Walter Reed Biosystematics Unit
[accessed April 30, 2020]. Available from: http://www.mosquitocatalog.org.
Zapata-Peniche
A,
Manrique-Saide
P,
Rebollar-Téllez
EA,
Che-Mendoza
A,
Dzul-Manzanilla
F.
2007
.
Identificación de larvas de mosquitos (Diptera: Culicidae) de Mérida, Yucatán, México y sus principales criaderos
.
Rev Bioméd
18
:
3
17
.

Author notes

1

Postgrado en Ciencias en Producción Agropecuaria, Universidad Autónoma Agraria Antonio Narro, Unidad Laguna, Periférico Raúl López Sánchez y Carretera a Santa Fe, 27054 Torreón, Coahuila, Mexico.

2

Departamento de Sistemática y Ecología Acuática, El Colegio de la Frontera Sur, Unidad Chetumal, Avenida del Centenario Km. 5.5, 77900 Chetumal, Quintana Roo, Mexico.

3

Departamento de Parasitología, Universidad Autónoma Agraria Antonio Narro, Unidad Laguna, Periférico Raúl López Sánchez y Carretera a Santa Fe, 27054 Torreón, Coahuila, Mexico.

4

Departamento de Enfermedades Transmitidas por Vector y Zoonosis, Servicios Estatales de Salud de Quintana Roo, Avenida Chapultepec No. 267, 77000 Chetumal, Quintana Roo, Mexico.