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. 2025 Mar 20;29:e00423. doi: 10.1016/j.parepi.2025.e00423

First report of Culicoides paraensis (Goeldi, 1905) (Diptera: Ceratoponidae) in Cuba: A new challenge for public health

Yanet Martínez Pérez a, Ariamys Companioni Ibáñez a, Zulema Menéndez Díaz a, Eric Camacho Acosta a, Mónica Sánchez González a, Nell Cox García a, Quenia del Rosario Casanova Drake b, Gladys Gutierrez-Bugallo a,1,⁎
PMCID: PMC11995114  PMID: 40230829

Abstract

Culicoides paraensis (Goeldi) (Diptera: Ceratoponidae) is considered the primary vector of Oropouche virus (Orthobunyavirus, Peribunyaviridae) in the American Tropics. Here, we report the first record of C. paraensis in Cuba, during the first known outbreak of Oropouche fever outside its endemic range in the Amazon region. Using human landing catches, we collected 98 specimens of C. paraensis in three Cuban provinces (Santiago de Cuba, Cienfuegos, and Havana), where Oropouche fever had been documented in humans. This species was not captured using various traps deployed at the sampling sites (BG-Sentinel, New Jersey traps, and CDC light traps), which may explain why C. paraensis had not been previously reported in Cuba. In North America, C. paraensis develops in wet treeholes, while in tropical regions, it uses cacao husks and banana stumps as larval habitats. However, the specific larval development sites for this species in Cuba are unknown. The capture of adult female C. paraensis in areas of active Oropouche virus circulation suggests their involvement in virus transmission in Cuba.

Keywords: Oropouche virus, No-see-ums, Orthobunyavirus, Biting midge, Ceratopogonidae, Cuba

Graphical abstract

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1. Introduction

The biting midge Culicoides paraensis (Goeldi, 1905) (Diptera: Ceratoponidae) is considered the main vector of Oropouche virus (OROV) (Orthobunyavirus, Peribunyaviridae) (LeDuc et al., 1981; Romero-Alvarez and Escobar, 2017). OROV transmission has been restricted to the Amazon basin for decades, where it typically alternates between vertebrates, such as non-human primates, sloths, and Culicoides paraensis (Pinheiro et al., 1981). The virus has also been isolated from several species of mosquito (Anderson et al., 1961) including Coquillettidia venezuelensis (Theobald, 1912), Aedes (Ochlerotatus) serratus (Theobald, 1901), and Culex quinquefasciatus Say, 1823 (Pinheiro et al., 1981).

Oropouche fever (a disease caused by OROV) rang the alarm of the Pan American Health Organization on February 2024 due to an increase in human cases in some Amazonian countries (Brazil, Bolivia, Peru, and Colombia), but also outside the usual range of viral activity (OPS/OMS, 2024a). By May 27, 2024, Cuba reported its first OROV outbreak in two provinces (Santiago de Cuba and Cienfuegos), which by August 2024 reached all 15 provinces with more than 500 confirmed cases (OPS/OMS, 2024b). This is the first outbreak caused by a Bunyavirus in Cuba (Benitez et al., 2024), thus the vectors responsible for its transmission on the island were unknown.

To date, 15 species of the Ceratopogonidae family have been recorded in Cuba (none of them identified as OROV vectors), mainly belonging to the genera Leptoconops (2), Forcipomyia (2), Bezzia (1), Nilobezzia (1), Monohelea (1), and Culicoides (8) (Gutsevich et al., 1969; Alayo and García, 1983; Castillo et al., 2014). However, the presence of C. paraensis in the country has not been reported. The list of Ceratopogonidae in Cuba was last updated in 1983 (Alayo and García, 1983), so given the unprecedented outbreak of Oropouche fever in Cuba, we aimed to identify ceratopogonid species in areas with active OROV transmission.

2. Materials and methods

2.1. Collection sites

From June to August 2024, collections were conducted at various sites in active OROV transmission provinces (Santiago de Cuba, Cienfuegos, and Havana), where residents complained about midge bites (Fig. 1). Both adult traps and human landing catches were used. BG-Sentinel traps (Biogents AG, Regensburg, Germany) with BG-Lure cartridges were deployed for 24 h, starting at 8:00 am. New Jersey and CDC light traps (J.W. Hock, Gainesville, USA) were set between 6:00 pm and 8:00 am. The traps were placed outside homes on a weekly basis throughout the sampling period. For human landing catches, two volunteers at each sampling site alternated using a hand aspirator once during the study period. The exposure time was 15 min, between 12:00 pm and 7:00 pm, based on local reports of biting activity occurring throughout the day.

Fig. 1.

Fig. 1

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Localities (in red dots) with active Oropouche virus transmission in three Cuban provinces (Havana, Cienfuegos, and Santiago de Cuba) where Ceratopogonids were capture from June to August 2024. Havana province is enlarged. 1- Santiago de Cuba (−75,809,394; 20,062844), 2- Songo La Maya (−75,640,324; 20,170,629), 3- Abreus (−80,56,155; 22,279,093), 4- Cienfuegos (−80,445,194; 22,154,802), 5- Boyeros (−82,372,236; 23,053445), 6- Diez de Octubre (−82,365,403; 23,092262), 7- Reparto Fraga (−82,481,413; 23,044497), 8- Novia del Mediodía (−82,475,358; 23,036501), 9- Guatao (−82,495,322; 23,002879), 10- Los Avioncitos (−82,457,675; 23,067297). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

2.2. Species identification

The collected specimens were preserved in 70 % ethanol. Subsequently, the morphological structures used in identification were clarified and mounted on microscope slides with Canada balsam using the technique described by Borkent and Spinelli, 2007. Morphological terminology here employed is based on Borkent, 2017 and Borkent et al., 2009. Assignment of Culicoides species to subgenus and species groups follows the system proposed by Felippe-Bauer et al., 2003 and Blosser et al., 2024, as no Cuban taxonomic key is available for this group.

The main morphologic characters considered for identification were the patterns of the wings, the sensory pit of the third segment of the maxillary palps, the coloration of the tibia of the third pair of legs, and the number and shape of the spermathecae. Identification was made at the National Reference Laboratory in the Vector Control Department of the Institute of Tropical Medicine Pedro Kouri (IPK), Havana, Cuba. Reference material was deposited in the IPK collection.

2.3. Ethical considerations

Biting midges were exclusively captured by trained personnel from the Vector Control Department of IPK. Written consents were obtained from every volunteer, after being clearly informed of the risks and benefits they took when involved in this study.

3. Results and discussion

A total of 98 female specimens of C. paraensis were collected by human landing catch. This biting midge species was not captured by any of the traps (BG-Sentinel, New Jersey traps, and CDC light traps) deployed at the sampling sites. Distribution by provinces was as follows: three from Santiago de Cuba, 21 from Cienfuegos, and 74 from Havana (Fig. 1). The number of specimens collected may not reflect the specie's abundance due to the vector control measures implemented by public health authorities at OROV transmission sites (Benitez et al., 2024).

The main morphological features observed in every specimen are shown in Fig. 2 and listed below: i) no pale spot anterior to base of mediocubital stem (Fig. 2a); ii) eyes broadly separated (Fig. 2b); iii) third palpal segment longer and more slender (PR 2.1–2.8) with pit deep and narrow, opening by a smaller pore (Fig. 2c); iv) spermathecae unequal sized, smaller spermatheca with duct stouter, not thread like, sclerotized ring long and curved (Fig. 2d).

Fig. 2.

Fig. 2

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Culicoides paraensis female parts collected in areas with active Oropouche virus transmission in Cuba. (a) Wing, (b) dorsal portion of head, (c) third palpal segment (d) spermathecae.

The recognition of all these traits allowed us to confirm, for the first time in Cuba, the occurrence of C. paraensis in 10 localities from three provinces in the east (Santiago de Cuba province), central (Cienfuegos province) and west (Havana province) parts of Cuba. This species belongs to the paraensis group that includes six other species: C. diversus Felippe-Bauer, C. peruvianus Felippe-Bauer; C. filiductus Wirth; C. quasiparaensis Clastrier; C. neoparaensis Tavares y Souza (Felippe-Bauer et al., 2003) and C. austroparaensis Spinelli (Spinelli et al., 2005).

It is unclear whether C. paraensis has been long present but undetected in Cuba or whether it was introduced and established in the recent past. Inhabitants in the collection areas indicated that numbers of biting midge bites have increased in recent years (since 2019). C. paraensis has a neotropical distribution, occurring from the south of the United States to Argentina (Blosser et al., 2024; Huerta et al., 2022; Felippe-Bauer et al., 2003). In the Antilles, C. paraensis has been recorded in, Trinidad (Wirth and Felippe-Bauer, 1989; Felippe-Bauer et al., 2003), Saint Vincent and the Grenadines, Grenada, St Andrews, and Barbados (Forattini, 1957). Therefore, its presence in Cuba is not unexpected.

This biting midge is a small forest insect about 1–3 mm in size. It exhibits diurnal hematophagic activity, mainly during the crepuscular period, and is an aggressive biter that is attracted to humans (Travassos da Rosa et al., 2017). C. paraensis larvae develop in a variety of moist habitats, particularly wet tree holes and other phytotelmata. Additionally, certain types of plantations (e.g. banana, cocoa) have been associated with a greater incidence of this midge since C. paraensis breeds in decaying vegetation resulting from the cultivation of these crops (Hoch et al., 1986; Felippe-Bauer et al., 2003; Sakkas et al., 2018). In Cuba, the Culicoides genus has been poorly studied in public health, mainly due to its limited role as a human pathogen vector. The recent OROV outbreak in the island sets a major challenge in characterizing C. paraensis biology, which is a determinant for designing vector control strategies. To accomplish that, biting midge capture methods should be improved to guarantee a safer collection method. In our case, adult traps like BG-Sentinel with BG-Lure cartridge, New Jersey traps, and CDC light traps located outdoors at different times in the same aforementioned collection sites did not result in any C. paraensis capture (data not shown). Further assays using other attractants like carbon dioxide, could favor the collection of this species (Venter et al., 2009; Blosser et al., 2024).

In conclusion, we reported the first identification of C. paraensis in three different Cuban regions. The presence of this species in localities with active OROV transmission and its known role as an OROV vectors abroad suggest its likely involvement in the Oropouche fever outbreak in Cuba. Further studies should be conducted to demonstrate and characterize its actual role as OROV vector in the Cuban context.

CRediT authorship contribution statement

Yanet Martínez Pérez: Writing – review & editing, Writing – original draft, Visualization, Methodology, Investigation, Formal analysis, Data curation, Conceptualization. Ariamys Companioni Ibáñez: Writing – review & editing, Writing – original draft, Validation, Supervision, Resources, Investigation, Formal analysis, Conceptualization. Zulema Menéndez Díaz: Writing – review & editing, Writing – original draft, Visualization, Validation, Methodology, Investigation, Formal analysis, Data curation. Eric Camacho Acosta: Writing – review & editing, Investigation. Mónica Sánchez González: Writing – review & editing, Visualization, Investigation. Nell Cox García: Writing – review & editing, Investigation. Quenia del Rosario Casanova Drake: Writing – review & editing, Investigation. Gladys Gutierrez-Bugallo: Writing – review & editing, Writing – original draft, Validation, Investigation, Conceptualization.

Declaration of competing interest

The authors declare no competing interests.

Acknowledgements

We are thankful to the Dirección Nacional de Vigilancia y Lucha Antivectorial (DNVLA) of the Cuban Ministry of Health for the logistic support during the sampling activities. We are most thankful to PAHO for their donation of traps and to their temporary consultant, Heron Huerta, for his assistance in identifying Culicoides species. Likewise, we want to thank Joaquim Pinto Nunes Neto from Evandro Chagas Institute for his guidance in Culicoides collection methods. We also appreciate the valuable suggestions made by professor Maria G. Guzman and María del C. Marquetti to the present article. Additionally, we are deeply grateful to Yosiel Molina for refining the English text. Finally, we appreciate the constructive comments provided by the anonymous reviewers.

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