﻿An updated catalogue of biting midges of the genus Culicoides Latreille, 1809 (Diptera, Ceratopogonidae) of Mexico and their known distribution by state

﻿Abstract An updated catalogue of Culicoides of Mexico is presented. It includes 86 species with their regional distribution and corresponding record references, known immature stages and associated pathogens. In addition, a taxonomic key for subgenera and species groups for Mexico is presented and an index of species by state is included.


Introduction
Species of the genus Culicoides Latreille, 1809 are tiny hematophagous dipterans, between 1 to 3 millimeters of length, and are known as "jejenes", "polvorines", "purrujas", or "chaquistes" in Spanish, and as "biting midges", "no-seeums", or "punkies" in English (Ibáñez-Bernal et al. 1996;Spinelli et al. 2005). This genus is the most diverse in the family Ceratopogonidae and is composed of 1,368 known extant species, classified into 33 subgenera, 38 species groups, and the remainder as miscellaneous (Borkent and Dominiak 2020;Borkent et al. 2022;Chatterjee et al. 2022;Labuschagne et al. 2023;Sarkar et al. 2023). Except for the regions of New Zealand and Antarctica, biting midges are distributed throughout the world and their populations occur in wetland, forest, agricultural, rural, and peri-urban areas, from sea level to 4,200 m of altitude (Wirth and Blanton 1959;Harrup et al. 2015).
Biting midges are a global concern because they cause direct and indirect damage to humans, domestic animals, and wildlife. Some species are vectors of pathogens, including viruses, bacteria, protozoa, and filariae (Vargas 1969;Borkent 2004) that infect different vertebrates, mainly birds and ruminant mammals, and produce important diseases such as Oropouche fever, Bluetongue disease, African horse sickness, Epizootic hemorrhagic disease, Schmallenberg disease (Mellor et al. 2000;Sick et al. 2019), as well as avian malaria by different species of Haemoproteus Kruse, 1890, Leucocytozoon Berestneff, 1904, Hepatocystis Levaditi & Schoen, 1932, and Trypanosoma Gruby, 1843(Valkiunas 2005. In addition, their high densities and often-irritating bites cause skin lesions, secondary infections, and allergies (Blanton and Wirth 1979;Ibáñez-Bernal et al. 2020) and can generate important economic losses in sectors related to recreation and tourism, forestry, and agriculture (Wirth and Blanton 1974;Borkent and Spinelli 2007).
In several regions of the world, the transmission of pathogens by different species of Culicoides directly affects human health and has a detrimental effect on the farming industry and wildlife conservation programs. Mansonellosis, caused by Mansonella filariae, affects regions in America and Africa, and Oropouche fever, caused by a virus of the same name affects Central and South American countries, both considered neglected diseases which are the most relevant human diseases in which a Culicoides species is involved as vector (Linley et al. 1983;Borkent 2004;Mediannikov and Ranque 2018;Romero-Alvarez and Escobar 2018). However, pathogens of veterinary importance, such as Bluetongue virus, Epizootic hemorrhagic virus, Schmallenberg virus, and avian haemosporidians, cause significant economic losses at local and regional levels in farm industry (Mills et al. 2017;Alkhamis et al. 2020;Marzal and García-Longoria 2020), mainly because of high animal mortality and morbidity, transport bans, trade restrictions, prevention and control costs, and management and conservation efforts directed at wildlife (Sick et al. 2019;Marzal and García-Longoria 2020).
Despite the important sanitary and economic damages caused by different species of Culicoides, in Mexico, they have been scarcely studied as compared with other hematophagous Diptera; given their global relevance, at present, the study of the genus in the country can be considered neglected. The current knowledge of Mexican species corresponds to the taxonomic description (Root and Hoffman 1937;Hoffman 1939;Vargas 1944Vargas , 1953aVargas , 1953bVargas , 1954Vargas , 1955Vargas , 1960Vargas , 1972Macfie 1948;Vargas and Wirth 1955;Spinelli and Huerta 2015) and distribution records (Wirth and Jones 1957;Wirth and Hubert 1960;Wirth and Blanton 1978;Wirth and Moraes 1979;Huerta 1996;Huerta et al. 2012Huerta et al. , 2020Huerta et al. , 2022, progressively compiled in different lists and catalogues. The first list of species from Mexico was elaborated by Vargas (1945) and included 14 species without a subgeneric classification. A decade later, the known richness was increased to 31 species by Fox (1955) in his catalog of hematophagous ceratopogonids of America and, later, to 50 species by Wirth (1974) in the "Catalog of the Diptera of America south of the United States", both of which already present a subgeneric classification of the genus. Ibáñez-Bernal et al. (1996) updated the richness of the family Ceratopogonidae in Mexico and specifically for the genus Culicoides, reporting 71 species, 13 subgenera, and eight endemic species; however, the identity of the species was not mentioned. The most recent catalog that most completely incorporated the known Culicoides fauna of Mexico, and its regional distribution was presented by Borkent and Spinelli (2000), in which they reported 69 species (eight endemic), 14 subgenera, and eight species groups. More recently, catalogues of the family Ceratopogonidae have corresponded to the Nearctic (Borkent and Grogan 2009) and Neotropical fauna (Borkent and Spinelli 2007), the two biogeographic regions that collide in Mexico (Griffiths 1980;Halffter 2003;Morrone 2005), but do not include all species known from Mexico. Particularly for the Neotropical Region, 49 species, 12 subgenera and 7 species groups have been reported, and for the Nearctic Region, 38 species, 10 subgenera and 3 species groups, respectively; neither of the two catalogues included the known endemic species of the country which were unknown at the time.
Mexico's biogeographic regions are important for Culicoides species distribution. The Nearctic and Neotropical Regions possess different habitats, with arid xerophyte vegetation and temperate forests in the north, and tropical forests in the south (Griffiths 1980). Culicoides species can be restricted to one region or occur in both. The "Mexican Transition Zone" is a vital area with various ecosystems and serving as a bridge between the two regions (Halffter 2003). It allows for the exchange of flora and fauna, and both regions share some biotic elements due to historical and ecological processes, but also there are conditions that promote endemism.
In recent years, the emergence and re-emergence of diseases caused by pathogens transmitted by different Culicoides species, such as the Schmallenberg virus and Bluetongue virus (Sick et al. 2019), has increased the interest of researchers and institutions and the need for their study worldwide. Vector species of Culicoides have already been reported in Mexico (Dampf 1936;Borkent and Spinelli 2007); however, their role as vectors in the country is uncertain. Mexico hosts an important vertebrate faunal diversity, the four North American migratory bird routes, and the largest migration of birds of prey in the world (Rappole et al. 1998) making it an important region where pathogens can be dispersed and maintained by biting midges, increasing the risk of emergence or re-emergence of zoonoses or wildlife diseases.
Vector-borne diseases are increasing their distribution and incidence, acquiring a more preponderant role in the maintenance of human welfare. Under this framework and with the scarce attention that historically has been given to the study of Culicoides in Mexico, it is evident and necessary to update the known information of the genus in the country. This work presents an update catalogue of the Culicoides of Mexico. It includes 86 species of 15 subgenera, ten species groups and four species not included in any group or subgenus (Table 1). It is arranged by subgenus and species, followed by the author(s) and the year of publication of the original description, their synonymies, and references. Subgenera and species groups are presented alphabetically, but species are classified according to the most recent proposal of Borkent and Dominiak (2020) and the assignment to the limai group of C. luglani by Phillips (2022). For each species the original reference, type locality, and their regional distribution by state, with the corresponding record reference are also presented. In addition, a key for subgenera and species groups and an index of species by state are presented.

Conclusions
Expanding and updating the knowledge of insect vectors is essential for the creation, implementation, and improvement of surveillance and population control programs. The number of Culicoides species present in Mexico represents 6% of the known species worldwide, 57% of the Nearctic species and 29% of the Neotropical species. In addition, 11 species are endemic. These endemic species have adapted and diversified according to the topography, soil, and altitudinal gradients of the country and are concentrated in some states such as Mexico City, Michoacán, Veracruz, and Chiapas where more Culicoides endemics are known in areas 2,000 meters above sea level. However, the alteration of natural ecosystems by human activities and the scarcity of updated data makes the actual distribution of endemic Culicoides species uncertain. Therefore, it is essential to understand the processes that originate and sustain diversity in these areas, which are subject to rapid changes in climate and habitats. Mexico City is a special case, as it harbors more endemic Culicoides species, but it is also an area with strong anthropogenic and demographic pressure, which generates uncertainty about the current distribution of these species. This is especially important in sites such as Chapultepec and San Jacinto.
The Nearctic Region includes North America, covering arid and temperate zones in northern Mexico, such as Baja California, Chihuahua, and Nuevo León, as well as the central region of Mexico, which includes Mexico City and Puebla. On the other hand, the Neotropical Region extends through the tropical and subtropical zones of southern Mexico, and a large part of the coastal region of the Pacific and Gulf of Mexico.
The distribution of Culicoides species in Mexico is classified into four main categories: Nearctic, Neotropical, broad distribution in the New World, and endemic. Of the species present in the country, 50% are distributed in the Nearctic Region, 77% in the Neotropical Region, 27% in both regions, and 13% are endemic. A wide variety of species distribution can be observed. For example, the subgenera C. Although C. (Hoffmania) is also common in this Region, the presence of C. in signis has been recorded in the Nearctic and represents an important health risk.
In addition, C. (Glaphiromyia) is a subgenus mainly endemic to Mexico, which makes it of special interest from a biogeographical perspective since species of this subgenus have been described in the transition zone of central Mexico.
Of Mexico's 32 states, Culicoides species have been recorded in only 25. Veracruz and Chiapas had the highest richness of biting midges. The subgenus Drymodesmyia is the best represented in the country with 14 species recorded, followed by the subgenus Hoffmania, represented by nine species. It should be noted that most of the records made in the country are the result of collection events more than half a century old and few records have been made in recent years; in addition, there are species that have not been collected since they were recorded; thus, the occurrence and distribution of several species should be reevaluated.
In general, the immature stages of Culicoides species are largely unknown and represent an important potential area of study. The immature stages of 30% of species present in Mexico are known. The egg stage is known for 5.8% of the species, while both larval and pupal stages for 27%. On the other hand, 15 species (17.4%) have been associated with different pathogens and therefore represent a potential risk as vectors in the country. Of these, eight species were associated with viruses, among which C. sonorensis, C. insignis and C. paraensis stand out for their greatest impact on human and animal health. The presence of these species in the country poses a greater health risk; therefore, it is vital to increase surveillance efforts to prevent possible disease outbreaks, especially in regions of high susceptibility, such as those with high livestock production. In addition, six species were associated with the transmission of nematodes and six species with protozoa, particularly Haemosporida.
The dichotomous keys presented in this work are the first to specifically focus on the Culicoides fauna of Mexico. Previously, it was necessary to consult several studies to identify the species present in the country. However, since the current subgeneric classification of Culicoides species could include inconsistencies and is in urgent need of revision, it is likely that these keys should help update the knowledge of the genus in the country.
Lastly, it is important to note that due to the physiographic, climatic, and topographic characteristics of the country, the great variety of ecosystems with conditions like those of other neotropical countries, as well as the lack of systematic and faunistic studies that address the spatial and temporal changes of the group, it can be inferred that the species richness of Culicoides in the country is far from being elucidated. Wirth WW, Blanton FS (1955a) Studies in Panama Culicoides (Diptera, Heleidae) IV. Descriptions of three new species. Bulletin of the Brooklyn Entomological Society 50: