We provide the first records of 8 species of biting midges in the genus Culicoides (Diptera: Ceratopogonidae) in a wide latitudinal gradient of the Yungas Ecoregion in Argentina and the Chaco Ecoregion in Bolivia, including a map of their distribution, and an updated checklist of species in the study area. Additional locality records were obtained from published articles and from specimens collected in these and other ecoregions in both countries. Included are the first Argentinean records of Culicoides crescentis Wirth & Blanton and C. pampaensis Spinelli & Wirth from Salta Province; C. caridei Brèthes, C. crescentis, C. guttatus Coquillett, C. insignis Lutz, C. pampaensis, and C. venezuelensis Ortiz & Mirsa from Jujuy Province, and C. saltaensis Spinelli & Wirth and C. pampaensis from Tucumán Province. In addition, the first records of C. brasilianum Forattini, C. crescentis, and C. guttatus are provided from Bolivia.
Biting midges of the genus Culicoides Latreille (Diptera: Ceratopogonidae) are the most diverse group of the family Ceratopogonidae, which includes 1,366 extant worldwide species, 266 of which occur in the Neotropics (Borkent & Spinelli 2007; Borkent 2014a). Presently, 53 species of Culicoides are known from Argentina (Spinelli & Wirth 1993; Spinelli et al. 2005; Veggiani Aybar et al. 2010) including 2 new species recently described by Spinelli et al. (2013) from northwestern Argentina. Conversely, the Culicoides fauna of Bolivia is poorly known, with only 18 species reported from this country (Spinelli et al. 2009; Veggiani Aybar et al. 2011).
The diversity and abundance of Neotropical species in this genus and their well-known pestiferous hematophagous habits include some species that are vectors of diseases in humans and other vertebrates (Mellor et al. 2000; Borkent 2004). Culicoides species impact public health due to their nuisance biting by adult females, which can cause cutaneous pruritis with resulting formation of wheals, flares, and permanent scarring (Sherlock & Guitton 1965; Linley et al. 1983; Felippe- Bauer & Sternheim 2008). Furthermore, Culicoides species are vectors of important arboviruses affecting cattle, such as bluetongue virus, equine encephalitis virus, epizootic hemorrhagic disease virus, African horse sickness virus, Akabane virus, bovine ephemeral fever virus, and Schmallenberg virus (Mellor et al. 2000; Borkent 2004; Carpenter et al. 2013). Culicoides species have also been implicated in the transmission of certain pathogens to humans, such as Mansonella nematodes, Leishmania flagellates and Oropouche virus, among others (Mellor et al. 2000; Ronderos et al. 2003; Borkent 2004; Seblova et al. 2012; Slama et al. 2014).
Herein, we provide the first records of 8 species of Culicoides from northwestern Argentina and southwestern Bolivia as well as an updated list of Culicoides in both of these countries.
Materials and Methods
SAMPLING SITES
We collected adult Culicoides during 2010–2013 at the following 10 localities in the subtropical mountainous rainforest ecoregion in northwestern Argentina and in the Chaco Ecoregion in southwestern Bolivia: Campo Quijano and Reserva Nacional Pizarros (Salta Province), Libertador General San Martín and Yuto (Jujuy Province), and Alpachiri, Santa Ana, and Villa Batiruana (Tucumán Province) in Argentina; and Pozo del Bermejo (Aniceto Arce Province), Itavicua and Campo Verde (Gran Chaco Province) in Bolivia.
COLLECTION AND PROCESSING OF CULICOIDES SPECIMENS
Specimens were collected with CDC light traps with UV- or white-lights baited with CO2 in anthropogenic and forested environments, from early dusk until morning of the next day, (17:00 to 07:00; 4 trappings/site/month).Collected specimens were frozen, sorted to morpho-species, preserved in 70% alcohol, and those difficult to accurately identify were dissected and slide-mounted in Canada balsam. Slide-mounted specimens were examined in detail with a binocular compound microscope, and identified by comparing them with illustrations, descriptions, and keys in Wirth & Blanton (1959) and Spinelli et al. (2005), as well as wing photos of females in the Neotropical wing atlas by Wirth et al. (1988).
Identification of species was based on female wing patterns, the shapes of male and female reproductive organs, the size and shape of female sensory pits on palpal segment 3, and the distribution of sensilla coeloconica female antennal flagellomeres. Assignment of species to subgenera and species groups followed the system proposed by Borkent (2014b).Voucher specimens were deposited in the entomological collection of the Instituto-Fundación Miguel Lillo (IFML), Tucumán Province, Argentina. Additional locality records for Tables 1 and 2 were obtained from published articles and specimens in IFML and the Museo de La Plata (MLPA), Argentina.
Results
In total, 4,128 Culicoides specimens were collected in the 2 ecoregions and 16 species were identified. Of these, 81 specimens (74 females, 7 males) belonging to 8 species are the first records from northwestern Argentina and Bolivia. Their taxonomic status, geographical distribution, type of trap with which they were collected, and surrounding environments are detailed below.
Subfamily Ceratopogoninae Newman
Tribe Culicoidini Kieffer
Genus Culicoides Latreille
Subgenus Cotocripus Brèthes
Culicoides (Cotocripus) caridei Brèthes
Current distribution: Argentina (Buenos Aires and Río Negro Provinces), Brazil, and Uruguay.
New records: ARGENTINA: Jujuy Province, Yuto (23°38′S, 64°28′W), Ledesma Department, XI-2012, CDC traps with white-light, anthropogenic environment, Veggiani Aybar & Dantur Juri coll., 2 females, 1 male, Veggiani Aybar det.; Libertador General San Martín (23°48′S, 64°48′W), Ledesma Department, X-2012, CDC traps with UV-light, anthropogenic environment, Veggiani Aybar & Dantur Juri coll., 6 females, 2 males, Veggiani Aybar det.
Subgenus Drymodesmyia Vargas
Culicoides (Drymodesmyia) saltaensis Spinelli & Wirth
Current distribution: Argentina (Salta and La Rioja Provinces).
New records: ARGENTINA: Tucumán Province, Alpachiri (27°20′S, 65°46′W), Chicligasta Department, XII-2012, III-2013, CDC traps with UV-light, anthropogenic environment and forested, Veggiani Aybar coll., 4 females, 1 male, Veggiani Aybar det.; Santa Ana (27°28′S, 65°39′W), Río Chico Department, IX-2012, CDC traps with UV-light, anthropogenic environment, Veggiani Aybar coll., 2 females, Veggiani Aybar det.; Villa Batiruana (27°38S, 65°44′W), Juan Bautista Alberdi Department, XII-2012, CDC traps with UV-light, anthropogenic environment, Veggiani Aybar coll., 2 females, Veggiani Aybar det.
Subgenus Haematomyidium Goeldi
Culicoides (Haematomyidium) pampaensis Spinelli & Wirth
Current distribution: Argentina (Catamarca, La Pampa, and Salta Provinces).
New records: ARGENTINA: Jujuy Province, Libertador General San Martín (23°48′S, 64°48′W), Ledesma Department, XI-2012, CDC traps with UV-light, anthropogenic environment, Veggiani Aybar & Dantur Juri coll., 2 females, Veggiani Aybar det. Salta Province, San José de Metán (25°30′S, 64°58′W), Metán Department, IX-2013, CDC traps with white-light, anthropogenic environment, Veggiani Aybar & Dantur Juri coll., 2 females, Veggiani Aybar det.
Subgenus Hoffmania Fox
Culicoides (Hoffmania) brasilianum Forattini
Current distribution: Argentina (Misiones Province) and Brazil.
New records: BOLIVIA: Aniceto Arce Province, Pozo del Bermejo (22°35′S, 64°26′W), Tarija Department, VIII-2012, CDC traps with UV-light, anthropogenic environment and forested , Veggiani Aybar coll., 2 females, Veggiani Aybar det.; Gran Chaco Province, Itavicua (21°50′S, 63°38′W),Tarija Department, X-2013, CDC traps with UV-light, anthropogenic environment, Laci & Carrizo coll., 1 female,Veggiani Aybar det.
Culicoides (Hoffmania) guttatus Coquillett
Current distribution: Argentina (Corrientes, Salta and Tucumán Provinces), Brazil, Ecuador, Paraguay, Surinam, and Venezuela.
New records: ARGENTINA: Jujuy Province, Yuto (23°38′S, 64°28′W), Ledesma Department, XI-2012, CDC traps with UV-light and white-light, anthropogenic environment, Veggiani Aybar & Dantur Juri coll., 3 females, 1 male, Veggiani Aybar det. BOLIVIA: Gran Chaco Province, Itavicua (21°50′S, 63°38′W), Tarija Department, X-2013, CDC traps with UV-light, anthropogenic environment, Laci & Carrizo coll., 2 females, Veggiani Aybar det.; Campo Verde (21°52′S, 63°34′W), Tarija Department, X-2013, CDC traps with UV-light and white-light, anthropogenic environment, Laci & Carrizo coll., 5 females, Veggiani Aybar det.
Culicoides (Hoffmania) insignis Lutz
Current distribution: Argentina (Buenos Aires, Corrientes, Salta, and Tucumán Provinces), Central America and Caribbean, México, and USA.New records: ARGENTINA: Jujuy Province, Libertador General San Martín (23°48′S, 64°48′W), Ledesma Department, XI-2012, I-2010, CDC traps with UV-light and white-light, anthropogenic environment and forested, Veggiani Aybar & Dantur Juri coll., 15 females, Veggiani Aybar det.; Yuto (23°38′S, 64°28′W), Ledesma Department, XI-2012, CDC traps with UV-light and white-light, anthropogenic environment, Veggiani Aybar & Dantur Juri coll., 9 females, 1 male, Veggiani Aybar det.
Table 1.
Updated checklist of Culicoides species in northwestern Argentina.
Table 2.
Updated checklist of Culicoides species in Bolivia.
Subgenus Psychophaena
Culicoides (Psychophaena) venezuelensis Ortiz & Mirsa
Current distribution: Argentina (Entre Ríos, Salta, and Tucumán Provinces), Bolivia (Aniceto Arce Province), Brazil, Ecuador, Chile, Colombia, Costa Rica, Panamá, Paraguay, and Uruguay.
New records: ARGENTINA: Jujuy Province, Yuto (23°38′S, 64°28′W), Ledesma Department, XI-2012, CDC traps with UV-light and white-light, anthropogenic environment, Veggiani Aybar & Dantur Juri coll., 12 females, 1 male, Veggiani Aybar det.
Subgenus unplaced
daedalus group
Culicoides crescentis Wirth & Blanton
Current distribution: Argentina (Salta and Tucumán Provinces), Mexico to Colombia.
New records: ARGENTINA: Jujuy Province, Libertador General San Martín (23°48′S, 64°48′W), Ledesma Department X-2012, CDC traps with white-light, anthropogenic environment, Veggiani Aybar & Dantur Juri coll., 1 female, Veggiani Aybar det. Salta Province, Campo Quijano (24°54′S, 65°41′W), Rosario de Lerma Department, X-2009, traps with UV-light, anthropogenic environment, Veggiani Aybar coll., 2 females, Veggiani Aybar det.; Reserva Nacional Pizarros (24°10′S, 64°03′W), Anta Department, I-2012, traps with UV-light, forested environment, Laci & Carrizo coll., 2 females, Veggiani Aybar det. BOLIVIA: Aniceto Arce Province, Pozo del Bermejo (22°35′S, 64°26′W), Tarija Department, VIII-2012, CDC traps with UV-light, forested environment, Veggiani Aybar & Dantur Juri coll., 2 females, Veggiani Aybar det.
Discussion
The objective of this study was to present the geographical distribution of the Culicoides fauna, extending its range of distribution in the subtropical mountainous rainforest ecoregion of Argentina and in the Chaco Ecoregion of Bolivia, including anthropogenic and forested environments. Other surveys of the genus Culicoides in this area were by Veggiani Aybar et al. (2010, 2011, 2012).
Of the species recorded, only C. insignis and C. venezuelensis have been incriminated in the transmission of diseases of veterinary importance (Ronderos et al. 2003; Perruolo 2009). For example, C. insignis has been reported as a vector of bluetongue virus in northeastern Argentina (Gorch et al. 2002; Ronderos et al. 2003). The discovery of this potential vector in the Yungas Ecoregion is of vital importance for developing health and veterinary measures aimed at minimizing the effect of this disease in this and surrounding areas.
Acknowledgments
We thank M. Zaidenberg and E. Laci, C. Laci, and D. Carrizo, Chief and Technicians of Coordinación Nacional de Control de Vectores, Ministerio de Salud de la Nación, for their collaboration during field work. We also give special thanks to William L. Grogan, Jr., Research Associate Florida State Collection of Arthropods, Florida Deptartment of Agriculture and Consumer Services for invaluable comments that helped to improve the manuscript.
