Morphological Aberrations of the Dirofilariasis, Sindbis Fever and West Nile Fever Vector Culex Theileri (Diptera: Culicidae) in Iran
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Abstract
Background: Culex theileri (Diptera: Culicidae) is a known vector of pathogens that cause dirofilariasis, Sindbis fever and West Nile fever in Iran. The species is one of the country’s most abundant and widely distributed species.
Methods: In order to conduct a faunistic and bionomic study of mosquitoes, larval collection was carried out in Chahar Mahal and Bakhtiari Province of western Iran using dipping method.
Results: In total, some 2096 larvae of Cx. theileri were identified. Among the larvae, 1024 (48.9%) displayed aberrations and anomalies in the development of cranial seta 1-C (preclypeal seta). Morphological aberrations and anomalies of seta 1-C in the third- and fourth-instar larvae and abdominal terga of the adults of Cx. theileri collected in Iran are discussed and illustrated.
Conclusion: More studies are needed throughout the distribution of Cx. theileri to analyze the variation of the species, especially using both morphological and molecular data.
1- Harbach RE (2022) Mosquito Taxonomic Inventory. Available at: http://mosquito-taxonomic-inventory.info/ (accessed 26 Jan 2022).
2- Harbach RE (1988) The mosquitoes of the subgenus Culex in southwestern Asia and Egypt (Diptera: Culicidae). Contrib Am Entomol Inst. 24(1): 1–240.
3- Azari-Hamidian S, Norouzi B, Harbach RE (2019) A detailed review of the mosquitoes (Diptera: Culicidae) of Iran and their medical and veterinary importance. Acta Trop. 194: 106–122.
4- Ventim R, Ramos JA, Osorio H, Lopes RJ, PeresTris J, Mendes L (2012) Avian malaria infections in western European mosquitoes. Parasitol Res. 111(2): 637–645.
5- Inci A, Yildirima A, Njabo KY, Duzlu O, Biskin Z, Ciloglu A (2012) Detection and molecular characterization of avian Plasmodium from mosquitoes in central Turkey. Vet Parasitol. 188(1–2): 179–184.
6- Ferraguti M, Martınezde la Puente J, Munoz J, Roiz D, Ruiz S, Soriguer R, Figuerola J (2013) Avian Plasmodium in Culex and Ochlerotatus mosquitoes from southern Spain: effects of season and host-feeding source on parasite dynamics. PLOS One. 8(6): e66237.
7- Santa-Ana M, Khadem M, Capela R (2006) Natural infection of Culex theileri (Diptera: Culicidae) with Dirofilaria immitis (Nematoda: Filarioidea) on Madeira Island, Portugal. J Med Entomol. 43(1): 104–106.
8- Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Abai MR, Mobedi I, Linton YM, Harbach RE (2009) Distribution and ecology of mosquitoes in a focus of dirofilariasis in northwestern Iran, with the first finding of filarial larvae in naturally infected local mosquitoes. Med Vet Entomol. 23(2): 111–121.
9- Morchón R, Bargues MD, Latorre-Estivalis JM, Pou-Barreto C, Melero-Alcibar R, Moreno M, Valladares B, Molina R, Montoya-Alonso JA, Mas-Coma S, Simón F (2011) Molecular characterization of Culex theileri from Canary Islands, Spain, a potential vector of Dirofilaria immitis. J Clinic Experiment Pathol. S3: 1–7.
10- McIntosh BM, Jupp PG, Dickinson DB, McGillivray GM, Sweetnam J (1967) Ecological studies on Sindbis and West Nile viruses in South Africa. I. Viral activity as revealed by infection of mosquitoes and sentinel fowls. S Afr J Med Sci. 32 (1): l–l4.
11- Shahhosseini N, Moosa-Kazemi SH, Sed-aghat MM, Wong G, Chinikar S, Hajivand Z, Mokhayeri H, Nowotny N, Kayedi MH (2020) Autochthonous transmission of West Nile virus by a new vector in Iran, vector-host interaction modeling and virulence gene determinants. Viruses. 12 (12): 1449.
12- Jupp PG, McIntosh BM, Brown RG (1966) Laboratory transmission experiments with West Nile and Sindbis viruses and Culex (Culex) theleri Theobald. S Afr J Med Sci. 31(3): 95–97.
13- Hanafi-Bojd AA, Motazakker M, Vatandoost H, Dabiri F, Chavshin AR (2021) Sindbis virus infection of mosquito species in the wetlands of northwestern Iran and modeling the probable ecological niches of SINV vectors in the country. Acta Trop. 220: 105952.
14- Wang HY, Takasaki T, Fu SH, Sun XH, Zhang HL, Wang ZX, Hao ZY, Zhang JK, Tang Q, Kotaki A, Tajima S, Liang XF, Yang WZ, Kurane I, Liang GD (2007) Molecular epidemiological analysis of Japanese encephalitis virus in China. J Gen Virol. 88(3): 885–894.
15- Gear J, de Meillon B, Le Roux AF, Kof-sky R, Rose Innes R, Steyn JJ, Oliff WD, Schulz KH (1955) Rift Valley fever in South Africa. A study of the 1953 outbreak in the Orange Free State, with special reference to the vectors and possible reservoir hosts. S Afr Med J. 29(22): 514–518.
16- McIntosh BM, Jupp PG, Dos Santos I, Barnard BJH (1980) Vector studies on Rift Valley fever virus in South Africa. S Afr Med J. 58(3): 127–132.
17- Cella E, Benvenuto D, Donati D, Garilli F, Angeletti S, Pascarella S, Ciccozzi M (2019) Phylogeny of Culex theileri virus flavivirus in Spain, Myanmar, Portugal and Turkey. Asian Pacific J Trop Med. 12(5): 216–223.
18- Calzolari M, Ze-Ze L, Ruzek D, Vazquez A, Jeffries C, Defilippo F, Osorio HC, Kilian P, Ruiz S, Fooks AR, Maioli G, Amaro F, Tlusty M, Figuerola J, Med-lock JM, Bonilauri P, Alves MJ, Sebesta O, Tenorio A (2012) Detection of mosquito-only flaviviruses in Europe. J Gen Virol. 93(6): 1215–1225.
19- Parreira R, Cook S, Lopes A, Pedro de Matos A, Paulo Gouveia de Almeida A, Piedade J, Esteves A (2012) Genetic characterization of an insect-specific flavivirus isolated from Culex theileri mosquitoes collected in southern Portugal. Virus Res. 167(2): 152–161.
20- Ergünay K, Litzba N, Brinkmann A, Günay F, Kar S, Öter K, Örsten S, Sarıkaya Y, Alten B, Nitsche A, Linton, YM (2016) Isolation and genomic characterization of Culex theileri flaviviruses in field-collected mosquitoes from Turkey. Infect Genet Evol. 46: 138–147.
21- de Pinho Mixao V, Mendes AM, Mauricio IL, Calado MM, Novo MT, Belo S, Al-meida APG (2016) Molecular detection of Wolbachia pipientis in natural populations of mosquito vectors of Dirofilaria immitis from continental Portugal: first detection in Culex theileri. Med Vet Entomol. 30: 301–309.
22- Bozorg-Omid F, Oshaghi MA, Vahedi M, Karimian F, Seyyed-Zadeh SJ, Chavshin AR (2020) Wolbachia infection in West Nile virus vectors of northwest Iran. Appl Entomol Zool. 55(1): 105–113.
23- Lewis DJ (1956) The Culex mosquitoes of the Sudan. Bull Entomol Res. 47(4): 703–721.
24- Bedford GAH (1915) A curious mosqui-to. Trans R Soc S Afr. 4(1): 143–144.
25- Sanchez-Murillo JM, Alarcon-Elbal PM, Gonzalez-Lopez M, Delacour-Estrella S, Lucientes J (2013) Description of two gynandromorphs of Culex theileri from Extremadura, Spain. J Am Mosq Control Assoc. 29(1): 61–63.
26- Demirci B, Lee Y, Lanzaro GC, Alten B (2012) Altitudinal genetic and morphometric variation among populations of Culex theileri Theobald (Diptera: Culicidae) from northeastern Turkey. J Vect Ecol. 37(1): 197–209.
27- Demirci B, Lee Y, Lanzaro GC, Alten B (2012) Identification and characterization of single nucleotide polymorphisms (SNPs) in Culex theileri (Diptera: Cu-licidae). J Med Entomol. 49(3): 581–588.
28- Azari-Hamidian S, Harbach RE (2017) Aberrations in the larval chaetotaxy of mosquitoes (Diptera: Culicidae) of Iran and a taxonomic note on the seta 1-C (preclypeal seta) of Culex in southwestern Asia. J Nat Hist. 51(1–2): 51–70.
29- Zaim M (1987) The distribution and larval habitat characteristics of Iranian Culicinae. J Am Mosq Cont Assoc. 3(4): 568–573.
30- Azari-Hamidian S, Abai MR, Arzamani K, Bakhshi H, Karami H, Ladonni H, Harbach RE (2011) Mosquitoes (Diptera: Culicidae) of North Khorasan Province, northeastern Iran, and the zo-ogeographic affinities of the Iranian and Middle Asian mosquito fauna. J Entomol. 8(3): 204–217.
31- Saghafipour A, Abai MR, Farzinnia B, Nafar R, Ladonni H, Azari-Hamidian S (2012) Mosquito (Diptera: Culicidae) fauna of Qom Province, Iran. J Arthropod Borne Dis. 6(1): 54–61.
32- Sofizadeh A, Shoraka HR, Mesgarian F, Ozbaki GM, Gharaninia A, Sahneh E, Dankoob R, Malaka A, Fallah S, Nemani S (2018) Fauna and larval habitats characteristics of mosquitoes (Diptera: Culicidae) in Golestan Province, north-east of Iran, 2014–2015. J Arthropod-Borne Dis. 12(3): 240–251.
33- Omrani SM, Azari-Hamidian S, Pourshahbazi G, Taghipour S (2015) Fauna and the distribution of mosquitoes (Diptera: Culicidae) in Chahar Mahal and Bakhtiari Province, 2011–2012. J Shahrekord Univ Med Sci. 16(6): 127–138 (in Persian).
34- Azari-Hamidian S, Norouzi B, Noorallahi A, Hanafi-Bojd AA (2018) Seasonal ac-tivity of adult mosquitoes (Diptera: Culicidae) in a focus of dirofilariasis and West Nile infection in northern Iran. J Arthropod-Borne Dis. 12(4): 398–413.
35- Omrani SM, Azari-Hamidian S (2020) Vertical distribution, biodiversity, and some selective aspects of the physico-chemical characteristics of the larval habitats of mosquitoes (Diptera: Culicidae) in Chaharmahal and Bakhtiari Province, Iran. Int J Epidemiol Res. 7(2): 74–91.
36- Azari-Hamidian S, Harbach RE (2009) Keys to the adult females and fourth-instar larvae of the mosquitoes of Iran (Diptera: Culicidae). Zootaxa. 20(78): 1–33.
37- Harbach RE, Knight KL (1980) Taxonomists’ Glossary of Mosquito Anatomy. Plexus Publishing, Marlton, NJ.
38- Harbach RE, Knight KL (1982) Corrections and additions to Taxonomists’ Glossary of Mosquito Anatomy. Mosq Syst. (for 1981). 13(2): 201–217.
2- Harbach RE (1988) The mosquitoes of the subgenus Culex in southwestern Asia and Egypt (Diptera: Culicidae). Contrib Am Entomol Inst. 24(1): 1–240.
3- Azari-Hamidian S, Norouzi B, Harbach RE (2019) A detailed review of the mosquitoes (Diptera: Culicidae) of Iran and their medical and veterinary importance. Acta Trop. 194: 106–122.
4- Ventim R, Ramos JA, Osorio H, Lopes RJ, PeresTris J, Mendes L (2012) Avian malaria infections in western European mosquitoes. Parasitol Res. 111(2): 637–645.
5- Inci A, Yildirima A, Njabo KY, Duzlu O, Biskin Z, Ciloglu A (2012) Detection and molecular characterization of avian Plasmodium from mosquitoes in central Turkey. Vet Parasitol. 188(1–2): 179–184.
6- Ferraguti M, Martınezde la Puente J, Munoz J, Roiz D, Ruiz S, Soriguer R, Figuerola J (2013) Avian Plasmodium in Culex and Ochlerotatus mosquitoes from southern Spain: effects of season and host-feeding source on parasite dynamics. PLOS One. 8(6): e66237.
7- Santa-Ana M, Khadem M, Capela R (2006) Natural infection of Culex theileri (Diptera: Culicidae) with Dirofilaria immitis (Nematoda: Filarioidea) on Madeira Island, Portugal. J Med Entomol. 43(1): 104–106.
8- Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Abai MR, Mobedi I, Linton YM, Harbach RE (2009) Distribution and ecology of mosquitoes in a focus of dirofilariasis in northwestern Iran, with the first finding of filarial larvae in naturally infected local mosquitoes. Med Vet Entomol. 23(2): 111–121.
9- Morchón R, Bargues MD, Latorre-Estivalis JM, Pou-Barreto C, Melero-Alcibar R, Moreno M, Valladares B, Molina R, Montoya-Alonso JA, Mas-Coma S, Simón F (2011) Molecular characterization of Culex theileri from Canary Islands, Spain, a potential vector of Dirofilaria immitis. J Clinic Experiment Pathol. S3: 1–7.
10- McIntosh BM, Jupp PG, Dickinson DB, McGillivray GM, Sweetnam J (1967) Ecological studies on Sindbis and West Nile viruses in South Africa. I. Viral activity as revealed by infection of mosquitoes and sentinel fowls. S Afr J Med Sci. 32 (1): l–l4.
11- Shahhosseini N, Moosa-Kazemi SH, Sed-aghat MM, Wong G, Chinikar S, Hajivand Z, Mokhayeri H, Nowotny N, Kayedi MH (2020) Autochthonous transmission of West Nile virus by a new vector in Iran, vector-host interaction modeling and virulence gene determinants. Viruses. 12 (12): 1449.
12- Jupp PG, McIntosh BM, Brown RG (1966) Laboratory transmission experiments with West Nile and Sindbis viruses and Culex (Culex) theleri Theobald. S Afr J Med Sci. 31(3): 95–97.
13- Hanafi-Bojd AA, Motazakker M, Vatandoost H, Dabiri F, Chavshin AR (2021) Sindbis virus infection of mosquito species in the wetlands of northwestern Iran and modeling the probable ecological niches of SINV vectors in the country. Acta Trop. 220: 105952.
14- Wang HY, Takasaki T, Fu SH, Sun XH, Zhang HL, Wang ZX, Hao ZY, Zhang JK, Tang Q, Kotaki A, Tajima S, Liang XF, Yang WZ, Kurane I, Liang GD (2007) Molecular epidemiological analysis of Japanese encephalitis virus in China. J Gen Virol. 88(3): 885–894.
15- Gear J, de Meillon B, Le Roux AF, Kof-sky R, Rose Innes R, Steyn JJ, Oliff WD, Schulz KH (1955) Rift Valley fever in South Africa. A study of the 1953 outbreak in the Orange Free State, with special reference to the vectors and possible reservoir hosts. S Afr Med J. 29(22): 514–518.
16- McIntosh BM, Jupp PG, Dos Santos I, Barnard BJH (1980) Vector studies on Rift Valley fever virus in South Africa. S Afr Med J. 58(3): 127–132.
17- Cella E, Benvenuto D, Donati D, Garilli F, Angeletti S, Pascarella S, Ciccozzi M (2019) Phylogeny of Culex theileri virus flavivirus in Spain, Myanmar, Portugal and Turkey. Asian Pacific J Trop Med. 12(5): 216–223.
18- Calzolari M, Ze-Ze L, Ruzek D, Vazquez A, Jeffries C, Defilippo F, Osorio HC, Kilian P, Ruiz S, Fooks AR, Maioli G, Amaro F, Tlusty M, Figuerola J, Med-lock JM, Bonilauri P, Alves MJ, Sebesta O, Tenorio A (2012) Detection of mosquito-only flaviviruses in Europe. J Gen Virol. 93(6): 1215–1225.
19- Parreira R, Cook S, Lopes A, Pedro de Matos A, Paulo Gouveia de Almeida A, Piedade J, Esteves A (2012) Genetic characterization of an insect-specific flavivirus isolated from Culex theileri mosquitoes collected in southern Portugal. Virus Res. 167(2): 152–161.
20- Ergünay K, Litzba N, Brinkmann A, Günay F, Kar S, Öter K, Örsten S, Sarıkaya Y, Alten B, Nitsche A, Linton, YM (2016) Isolation and genomic characterization of Culex theileri flaviviruses in field-collected mosquitoes from Turkey. Infect Genet Evol. 46: 138–147.
21- de Pinho Mixao V, Mendes AM, Mauricio IL, Calado MM, Novo MT, Belo S, Al-meida APG (2016) Molecular detection of Wolbachia pipientis in natural populations of mosquito vectors of Dirofilaria immitis from continental Portugal: first detection in Culex theileri. Med Vet Entomol. 30: 301–309.
22- Bozorg-Omid F, Oshaghi MA, Vahedi M, Karimian F, Seyyed-Zadeh SJ, Chavshin AR (2020) Wolbachia infection in West Nile virus vectors of northwest Iran. Appl Entomol Zool. 55(1): 105–113.
23- Lewis DJ (1956) The Culex mosquitoes of the Sudan. Bull Entomol Res. 47(4): 703–721.
24- Bedford GAH (1915) A curious mosqui-to. Trans R Soc S Afr. 4(1): 143–144.
25- Sanchez-Murillo JM, Alarcon-Elbal PM, Gonzalez-Lopez M, Delacour-Estrella S, Lucientes J (2013) Description of two gynandromorphs of Culex theileri from Extremadura, Spain. J Am Mosq Control Assoc. 29(1): 61–63.
26- Demirci B, Lee Y, Lanzaro GC, Alten B (2012) Altitudinal genetic and morphometric variation among populations of Culex theileri Theobald (Diptera: Culicidae) from northeastern Turkey. J Vect Ecol. 37(1): 197–209.
27- Demirci B, Lee Y, Lanzaro GC, Alten B (2012) Identification and characterization of single nucleotide polymorphisms (SNPs) in Culex theileri (Diptera: Cu-licidae). J Med Entomol. 49(3): 581–588.
28- Azari-Hamidian S, Harbach RE (2017) Aberrations in the larval chaetotaxy of mosquitoes (Diptera: Culicidae) of Iran and a taxonomic note on the seta 1-C (preclypeal seta) of Culex in southwestern Asia. J Nat Hist. 51(1–2): 51–70.
29- Zaim M (1987) The distribution and larval habitat characteristics of Iranian Culicinae. J Am Mosq Cont Assoc. 3(4): 568–573.
30- Azari-Hamidian S, Abai MR, Arzamani K, Bakhshi H, Karami H, Ladonni H, Harbach RE (2011) Mosquitoes (Diptera: Culicidae) of North Khorasan Province, northeastern Iran, and the zo-ogeographic affinities of the Iranian and Middle Asian mosquito fauna. J Entomol. 8(3): 204–217.
31- Saghafipour A, Abai MR, Farzinnia B, Nafar R, Ladonni H, Azari-Hamidian S (2012) Mosquito (Diptera: Culicidae) fauna of Qom Province, Iran. J Arthropod Borne Dis. 6(1): 54–61.
32- Sofizadeh A, Shoraka HR, Mesgarian F, Ozbaki GM, Gharaninia A, Sahneh E, Dankoob R, Malaka A, Fallah S, Nemani S (2018) Fauna and larval habitats characteristics of mosquitoes (Diptera: Culicidae) in Golestan Province, north-east of Iran, 2014–2015. J Arthropod-Borne Dis. 12(3): 240–251.
33- Omrani SM, Azari-Hamidian S, Pourshahbazi G, Taghipour S (2015) Fauna and the distribution of mosquitoes (Diptera: Culicidae) in Chahar Mahal and Bakhtiari Province, 2011–2012. J Shahrekord Univ Med Sci. 16(6): 127–138 (in Persian).
34- Azari-Hamidian S, Norouzi B, Noorallahi A, Hanafi-Bojd AA (2018) Seasonal ac-tivity of adult mosquitoes (Diptera: Culicidae) in a focus of dirofilariasis and West Nile infection in northern Iran. J Arthropod-Borne Dis. 12(4): 398–413.
35- Omrani SM, Azari-Hamidian S (2020) Vertical distribution, biodiversity, and some selective aspects of the physico-chemical characteristics of the larval habitats of mosquitoes (Diptera: Culicidae) in Chaharmahal and Bakhtiari Province, Iran. Int J Epidemiol Res. 7(2): 74–91.
36- Azari-Hamidian S, Harbach RE (2009) Keys to the adult females and fourth-instar larvae of the mosquitoes of Iran (Diptera: Culicidae). Zootaxa. 20(78): 1–33.
37- Harbach RE, Knight KL (1980) Taxonomists’ Glossary of Mosquito Anatomy. Plexus Publishing, Marlton, NJ.
38- Harbach RE, Knight KL (1982) Corrections and additions to Taxonomists’ Glossary of Mosquito Anatomy. Mosq Syst. (for 1981). 13(2): 201–217.
| Files | ||
| Issue | Vol 16 No 3 (2022) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v16i3.12036 | |
| Keywords | ||
| Anomalous; Abnormal; Character; Morphology; Variation | ||
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How to Cite
1.
Azari-Hamidian S, Omrani S-M. Morphological Aberrations of the Dirofilariasis, Sindbis Fever and West Nile Fever Vector Culex Theileri (Diptera: Culicidae) in Iran. J Arthropod Borne Dis. 2023;16(3):206–216.
