ABSTRACT
We provide new records of Culicoides paraensis from the Yucatan Peninsula. The anthropophilic biting midge C. paraensis is the main vector of Oropouche fever virus in South and Central America. We also report Culicoides poikilonotus for the 1st time in the Yucatan Peninsula and a key to identify the species in this region of Mexico.
The anthropophilic biting midge Culicoides paraensis (Goeldi) (Diptera: Ceratopogonidae) is the main vector of Oropouche fever (OROF), a zoonotic disease that can affect humans in South and Central America and caused by the orthobunyavirus Oropouche virus (OROV) (Romero-Alvarez and Escobar 2018). In May 2024, the Pan American Health Organization and the World Health Organization issued an epidemiologic alert for OROF in the region of the Americas because of an increase of in the detection of cases observed particularly in Bolivia, Brazil, Colombia, and Peru (OPS and OMS 2024).
Culicoides paraensis has a widespread distribution from Argentina (Borkent and Grogan 2009) to the southern USA (Wirth et al. 1985, 1988, Borkent and Spinelli 2007), including Mexico. Culicoides paraensis has been reported from central Mexico (San Luis Potosí) and the southern states of Chiapas, Tabasco, and Veracruz and Quintana Roo within the Yucatan Peninsula (Blanton and Wirth 1979, Wirth and Felippe-Bauer 1989, Huerta et al. 2012, 2022). Here, we report new records of C. paraensis for the 1st time from the state of Yucatan and another record from Quintana Roo, both in the Yucatan Peninsula. We also report Culicoides (Drymodesmyia) poikilonotus Macfie for the 1st time in the Yucatan Peninsula. Previously recorded distribution only included the Mexican states of Chiapas, Tabasco, and Veracruz (Huerta et al. 2012, 2022).
New record. Culicoides paraensis (Goeldi). Material examined. Country: Mexico. State: Yucatan. Locality: Reserva Ria Lagartos, Chiquila, Vegetation type: mangrove. Date: November 29, 1995. Collection method: human landing, Huerta Herón. Material: female slide mounted (Comisión Nacional de Biodiversidad 95 − 1005) deposited in Colección de Artrópodos con Importancia Médica (CAIM). State: Yucatan. Locality: Reserva Estatal Biocultural del Puuc (REBP), Oxkutzcab. Date: October 9, 2015. Collection method: Centers for Disease Control and Prevention (CDC trap), Juan Carlos Navarrete Carballo (JCNC). Material: male slide mounted (11 CERATOPOGONIDAE (CERA) 05C01) deposited in CAIM. State: Quintana Roo. Locality: Limones, Bacalar. Date: January 27, 2014. Collection method: CDC light (CDC trap) with blue led, 1800 h, Jorge Jesús Rodríguez Rojas. Material: female slide mounted deposited in CAIM.
New record. Culicoides poikilonotus Macfie. Material examined. Country: Mexico. State: Yucatan. Locality: REBP, Oxkutzcab. Date: October 7, 2015. Collection method: CDC (CDC trap), JCNC. Material: female (09CERA05C01D) deposited in CAIM. State: Yucatan. Locality: REBP, Oxkutzcab. Date: October 7, 2015. Collection method: CDC (CDC trap), JCNC. Material: male (10CERA03C01G) deposited in CAIM. State: Yucatan. Locality: REBP, Oxkutzcab. Date: October 9, 2015. Collection method: CDC (CDC trap), JCNC. Material: female (11CERA03C01A) deposited in CAIM.
To date, 13 species of Culicoides have been reported for 3 Mexican states of the Yucatan Peninsula (Table 1). We present a key to separate the species in this region. Culicoides paraensis can be separated by characters on wing spots of others similar species in the subgenus Haematomyidium in Mexico (Culicoides debilipalpis Lutz, Culicoides eadsi Wirth and Blanton, Culicoides ginesi Ortiz, and Culicoides kettlei Breidenbaugh and Mullens) principally by cell m1 with 3 pale spots and cell r3 with 4 distal pale spots narrowly separated from the wing margin. Culicoides paraensis has been collected with CDC traps, Malaise traps, and human landing catches in different regions of Mexico (Huerta et al. 2012, 2022).
To date, neither the presence of OROV nor any human case of OROF has been reported in Mexico. In June 2024, the Ministry of Health of Mexico issued a travel health notice for OROF to people traveling to Bolivia, Brazil, Colombia, Cuba, and Peru (Gobierno de México 2024). Nevertheless, it is very important to respond to the epidemiologic alert, activating diagnostic and surveillance protocols in humans, animal hosts, and vectors, including updates on the distribution of C. paraensis and active detection for OROV, because now no systematized surveillance is carried out in Mexico.
Vector prevention or control reactive measures or both, when needed, must be based on entomologic studies of the vectors involved in transmission, and entomologic collections should be expanded to detect C. paraensis and other potentially important species not yet considered of medical importance in the country. The Mexican Vector-Borne Diseases Program from Centro Nacional de Programas Preventivos y Control de Enfermedades, through the State Entomological Surveillance and Bioassay Units, will carry out targeted collections in different potential habitats and geographic areas to detect and characterize the ecology and behavior and to develop entomovirologic studies to detect OROV together with the National Institute of Epidemiological Diagnosis and Reference.
Some other species of Culicoides have been associated with the transmission of different arboviruses and filariae in the Neotropical region such as C. insignis Lutz, C. filarifer Hoffman, C. pusillus Lutz, C. furens (Poey), C. debilipalpis Lutz, and C. phlebotomus (Williston) (Borkent and Spinelli 2007). Culicoides poikilonotus has not been associated with any pathogen of medical importance. In Mexico, some studies have reported serologic and virologic evidence for bluetongue virus (BTV) transmission in domestic ruminants (Suzan et al. 1983, Teclaw et al. 1985, Scott et al. 1989, Hernandez et al. 1994, Martínez et al. 1999, Rojas-Anaya et al. 2022), and high rates of seropositivity against BTV and epizootic hemorrhagic disease virus in the northeastern region of Mexico (Lozano-Rendón et al. 2015, Martínez-Burnes et al. 2017, Merino et al. 2019). However, there are no studies confirming the vectorial competence of Culicoides species in Mexico.
The key to the adult Culicoides from the Yucatan Peninsula (primarily for females) is as follows:
1. Second radial cell completely or mostly included in a pale spot (Figs. 1 and 8) 2
–Second radial cell completely included in a dark spot (Figs. 2–7, 9–13) 3
2. Cell cua1 with small dark spot in middle portion (Fig. 1); vein r–m included in a pale spot neopulicaris
–Cell cua1 without small dark spot in the middle section (Fig. 8); vein r–m included in a dark spot insignis
3. Wing with a pale spot straddling the middle of vein M2 (Figs. 2, 9–12), some species included in widely pale area (Fig. 3); veins M1 and M2 usually with pale apex 8
–Wing without pale spot straddling vein M2 (Figs. 4–7, 13); veins M1 and M2 with dark apex 4
4. Cell m1 with pale spot (Figs. 4–7) 5
Cell m1 without pale spot (Fig. 13) pusillus
5. Cell m1 with 3 pale spots (Fig. 7); cell r3 with 4 pale spots narrowly separated from wing margin paraensis
–Cell m1 with 1 or 2 pale spots (Figs. 4–6); cell r3 with 3 pale spots 6
6. Hind femur with narrow subapical pale band poikilonotus (in part)
–Hind femur without subapical pale band 7
7. Base of medio-cubital fork included in dark spot (Fig. 5) debilipalpis
–Base of medio-cubital fork connected with adjacent pale area (Fig. 6) eadsi
8. Cell r3 with a small black spot behind 2nd radial cell(Fig. 12); 3 spermathecae arubae
–Cell r3 without a small black spot behind 2nd radial cell; 1 spermatheca or 2 spermathecae 9
9. Third palpal segment without sensory pit; 4th tarsal segment cordiform; tibial comb with 6–7spines phlebotomus
–Third palpal segment with sensory pit; 4th tarsal segment cylindrical; tibial comb with 4–5 spines 10
10. Mesonotum with distinctive pattern of punctiform brown dots 11
–Mesonotum without distinctive pattern of punctiform brown dots 12
11. Cell r3 with small, rounded, separated poststigmatic pale spot (Fig. 11); 3rd palpal segment with small,shallow sensory pit furens
–Cell r3 without small, rounded, separated poststigmatic pale spot (Fig. 10); 3rd palpal segment with deepsensory pit barbosai
12. Spermathecae saclike, elongate without sclerotized neck; wing with extensive pale areas (Fig. 3) loughnani
–Spermathecae oval, with sclerotized neck; wing without extensive pale areas (Figs. 2, 4) 13
13. Distal pale spot in cell r3 reaching anterior wing margin (Fig. 2) jamaicensis
–Distal pale spot in cell r3 not reaching anterior wing margin (Fig. 4) poikilonotus
Female, wings in dorsal view for Culicoides species. 1. C. neopulicaris; 2. C. jamaicensis; 3. C. loughnani; 4. C. poikilonotus; 5. C. debilipalpis; 6. C. eadsi; 7. C. paraensis; 8. C. insignis; 9. C. phlebotomus; 10. C. barbosai; 11. C. furens; 12. C. arubae; 13. C. pusillus. Scale = 0.5 mm.
Female, wings in dorsal view for Culicoides species. 1. C. neopulicaris; 2. C. jamaicensis; 3. C. loughnani; 4. C. poikilonotus; 5. C. debilipalpis; 6. C. eadsi; 7. C. paraensis; 8. C. insignis; 9. C. phlebotomus; 10. C. barbosai; 11. C. furens; 12. C. arubae; 13. C. pusillus. Scale = 0.5 mm.