Seasonal Activity of Adult Mosquitoes (Diptera: Culicidae) in a Focus of Dirofilariasis and West Nile Infection in Northern Iran

  • Shahyad Azari-Hamidian Research Center of Health and Environment, Guilan University of Medical Sciences, Rasht, Iran and School of Health, Guilan University of Medical Sciences, Rasht, Iran
  • Behzad Norouzi Research Center of Health and Environment, Guilan University of Medical Sciences, Rasht, Iran
  • Ayoob Noorallahi Department of Disease Control and Prevention, Health Vice-Chancellorship, Guilan University of Medical Sciences, Rasht, Iran
  • Ahmad Ali Hanafi-Bojd Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
Keywords: Dirofilaria, Flavivirus, Flaviviridae, Vectors, Iran


Background: Mosquito-borne arboviruses such as West Nile, dengue, Rift Valley fever, and Sindbis viruses and the nematode Dirofilaria are reported in Iran, but there is little information on the seasonal activity of their vectors in the country. We aimed to determine the seasonal activity of adult mosquitoes (Diptera: Culicidae) in a focus of diro-filariasis and West Nile infection in Guilan Province, northern Iran.Methods: Collections were carried out using light traps in seven counties at least two times from random sites and every two weeks from a fixed site (Pareh Village, Rudbar County) during Aug–Dec 2015 and Apr–Oct 2016.Results: Overall, 16327 adult mosquitoes comprising 18 species representing seven genera were identified. The most prevalent species were Cx. theileri (23.59%), Cx. tritaeniorhynchus (20.75%), Cx. pipiens (19.37%), Ae. vexans (18.18%), An. pseudopictus (10.92%) and An. maculipennis s.l. (5.48%). Aedes pulcritarsis and Cx. perexiguus were found for the first time in Guilan Province. The active season of adult mosquitoes extended from early May to early Oct in the fixed site. There was no significant regression between the abundance of adult mosquitoes and the meteor-ological data during active season in the fixed site (P> 0.05, R2= 0.31).Conclusion: Though no significant regression between the abundance of mosquitoes and the meteorological data was observed during active season, temperature and rice fields had a great influence in starting and ending active season in the region.


1. Hubálek Z, Halouzka J (1999) West Nile fever-a reemerging mosquito-borne vi-ral disease in Europe. Emerg Infect Dis. 5: 643–650.
2. Medlock JM, Snow KR, Leach S (2005) Potential transmission of West Nile virus in the British Isles: an ecological re-view of candidate mosquito bridge vec-tors. Med Vet Entomol. 19: 2–21.
3. Ahmadnejad F, Otarod V, Fallah MH, Low-enski S, Sedighi-Moghaddam R, Zavareh A, Durand B, Lecollinet S, Sabatier P (2011) Spread of West Nile virus in Iran: a cross-sectional serosurvey in equines, 2008–2009. Epidemiol Infect. 139: 1587–1593.
4. Chinikar S, Shah-Hosseini N, Mostafavi E, Moradi M, Khakifirouz S, Jalali T, Goya MM, Shirzadi MR, Zainali M, Fooks AR (2013) Seroprevalence of West Nile vi-rus in Iran. Vector-Borne Zoonotic Dis. 13: 586–589.
5. Pourmahdi Borujeni M, Ghadrdan Mashadi AR, Seifi Abad Shapouri MR, Zeinvand M (2013) A serological survey on anti-bodies against West Nile virus in horses of Khuzestan Province. Iran J Vet Med. 7: 185–191.
6. Naficy K, Saidi S (1970) Serological survey on viral antibodies in Iran. Trop Geogr Med. 2: 183–188.
7. Saidi S (1974) Viral antibodies in preschool children from the Caspian area, Iran. Iran J Publ Health. 3: 83–91.
8. Saidi S, Tesh R, Javadian E, Nadim A (1976) The prevalence of human infection of West Nile in Iran. Iran J Publ Health. 5: 8–14.
9. Sharifi Z, Mahmoodian M, Talebian A (2010) A Study of West Nile Virus In-fection in Iranian Blood Donors. Arch Iran Med. 13: 1–4.
10. Chinikar S, Javadi A, Ataei B, Shakeri H, Moradi M, Mostafavi E, Ghiasi SM (2012) Detection of West Nile virus ge-nome and specific antibodies in Iranian encephalitis patients. Epidemiol Infect. 140: 1525–1529.
11. Shah-Hosseini N, Chinikar S, Ataei B, Fooks AR, Groschup MH (2014) Phy-logenetic analysis of West Nile virus ge-nome, Iran. Emerg Infect Dis. 20: 1419–1421.
12. Meshkat Z, Chinikar S, Shakeri MT, Ma-navifar L, Moradi M, Mirshahabi H, Jalali T, Khakifirouz S, Shahhosseini N (2015) Prevalence of West Nile virus in Mashhad, Iran: A population-based study. Asia Pac J Trop Med. 8: 203–205.
13. Fereidouni SR, Ziegler U, Linke S, Niedrig M, Modirrousta H, Hoffmann B, Gro-schup H (2011) West Nile virus monitor-ing in migrating and resident water birds in Iran: are common coots the main res-ervoirs of the virus in wetlands? Vector-Borne Zoonotic Dis. 11: 1377–1381.
14. Bagheri M, Terenius O, Oshaghi MA, Mota-zakker M, Asgari S, Dabiri F, Vatandoost H, Mohammadi Bavani M, Chavshin AR (2015) West Nile virus in mosquitoes of Iranian wetlands. Vector-Borne Zoonotic Dis. 15: 750–754.
15. Shahhosseini N, Chinikar S, Moosa-Kazemi SH, Sedaghat MM, Kayedi MH, Luhken R, Schmidt-Chanasit J (2017) West Nile Virus lineage-2 in Culex specimens from Iran. Trop Med Inter Health. 22: 1343–1349.
16. Simon F, Siles-Lucas M, Morchon R, Gon-zalez-Miguel J, Mellado I, Carreton E, Montoya-Alonso JA (2012) Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clin Microbiol Rev. 25: 507–544.
17. Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Mobedi I, Abai MR (2007) Review of dirofilariasis in Iran. J Med Fac Guilan Univ Med Sci. 15(60): 102–113 (in Persian with English abstract).
18. Ranjbar-Bahadori S, Hekmatkhah A (2007) A study on filariosis of stray dogs in Garmsar. J Vet Res. 62: 73–76.
19. Akhtardanesh B, Radfar MH, Voosough D, Darijani N (2011) Seroprevalence of ca-nine heartworm disease in Kerman, south-eastern Iran. Comp Clin Pathol. 20: 573–577.
20. Khedri J, Radfar MH, Borji H, Azizzadeh M, Akhtardanesh B (2014) Canine heart-worm in [southeastern] of Iran with re-view of disease distribution. Iran J Par-asitol. 9: 560–567.
21. Heidari Z, Kia EB, Arzamani K, Sharifdini M, Mobedi I, Zarei Z, Kamranrashani B (2015) Morphological and molecular identification of Dirofilaria immitis from jackal (Canis aureus) in North Khorasan, northeast Iran. J Vector Borne Dis. 52: 329–333.
22. Mirahmadi H, Maleki A, Hasanzadeh R, Bagher Ahoo M, Mobedi I, Rostami A (2017) Ocular dirofilariasis by Dirofi-laria immitis in a child in Iran: a case report and review of the literature. Par-asitol Int. 66: 978–981.
23. Ashrafi K, Golchai J, Geranmayeh S (2010) Human subcutaneous dirofilariasis due to Dirofilaria (Nochtiella) repens: clini-cally suspected as cutaneous fascioliasis. Iran J Publ Health. 39: 105–109.
24. Ranjbar-Bahadori S, Veshgini A, Shirani D, Eslami A, Mohieddin H, Shemshadi B, Masooleh R (2010) Epidemiological as-pects of canine dirofilariasis in the north of Iran. Iran J parasitol. 6: 73–80.
25. Hosseini SH, Malmasi A, Aramon M (2010) Comparison of two diagnostic methods for Dirofilaria immitis: modified Knott test and ELISA. J Vet Med Lab. 2: 87–96 (in Persian with English abstract).
26. Malmasi A, Hosseini SH, Aramoon M, Bahonar A, Seifi HA (2011) Survey of canine Dirofilaria immitis infection in Caspian provinces of Iran. Iran J Vet Res. 12: 340–344.
27. 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 diro-filariasis in northwestern Iran, with the first finding of filarial larvae in naturally infected local mosquitoes. Med Vet En-tomol. 23: 111–121.
28. Azari-Hamidian S (2007) Checklist of Ira-nian mosquitoes (Diptera: Culicidae). J Vect Ecol. 32: 235–242.
29. Azari-Hamidian S, Harbach RE (2009) Keys to the adult females and fourth-in-star larvae of the mosquitoes of Iran (Dip-tera: Culicidae). Zootaxa. 2078: 1–33.
30. Oshaghi MA, Yaghobi-Ershadi MR, Shemshad Kh, Pedram M, Amani H (2008) The Anopheles superpictus com-plex: introduction of a new malaria vec-tor complex in Iran. Bull Soc Pathol Ex-ot. 101: 429–434.
31. Harbach RE (2013) The Phylogeny and Classification of Anopheles. In: Manguin S (Ed). Anopheles Mosquitoes - New In-sights into Malaria Vectors. InTech, Ri-jeka, Croatia, pp. 1–55.
32. Djadid ND, Jazayeri H, Gholizadeh S, Rad ShP, Zakeri S (2009) First record of a new member of Anopheles Hyrcanus Group from Iran: molecular identifica-tion, diagnosis, phylogeny, status of kdr resistance and Plasmodium infection. J Med Entomol. 46: 1084–1093.
33. Doosti S, Yaghoobi-Ershadi MR, Schaffner F, Moosa-Kazemi SH, Akbarzadeh K, Gooya MM, Vatandoost H, Shirzadi MR, Mostafavi E (2016) Mosquito surveil-lance and the first record of the invasive mosquito species Aedes (Stegomyia) al-bopictus (Skuse) (Diptera: Culicidae) in southern Iran. Iran J Publ Health. 45: 1064–1073.
34. Yaghoobi-Ershadi MR, Doosti S, Schaffner F, Moosa-Kazemi SH, Akbarzadeh K, Yaghoobi-Ershadi N (2017) Morpholog-ical studies on adult mosquitoes (Diptera: Culicidae) and first report of the potential Zika Virus vector Aedes (Stegomyia) un-ilineatus (Theobald, 1906) in Iran. Bull Soc Pathol Exot. 110: 116–121.
35. Azari-Hamidian S, Norouzi B, Noorallahi A (2017) Orthopodomyia pulcripalpis (Diptera: Culicidae), a genus and species new to the Iranian mosquito fauna, with a review of bionomical information. Zootaxa. 4299: 141–145.
36. Azari-Hamidian S (2011) Larval habitat characteristics of the genus Anopheles (Diptera: Culicidae) and a checklist of mosquitoes in Guilan Province, northern Iran. Iran J Arthropod-Borne Dis. 5: 37–53.
37. Azari-Hamidian S, Joeafshani MA, Rassaei A, Mosslem M (2002) Mosquitoes of the genus Aedes (Diptera: Culicidae) in Gui-lan. J Med Fac Guilan Univ Med Sci. 11: 29–39 (in Persian with English abstract)
38. Azari-Hamidian S (2007) Larval habitat characteristics of mosquitoes of the ge-nus Culex (Diptera: Culicidae) in Guilan Province, Iran. Iran J Arthropod-Borne Dis. 1: 9–20.
39. Nikookar SH, Moosa-Kazemi SH, Oshaghi MA, Vatandoost H, Yaghoobi-Ershadi MR, Enayati AA, Motevali-Haghi F, Zia-pour SP, Fazeli-Dinan M (2015) Biodi-versity of culicid mosquitoes in rural Neka township of Mazandaran Province, northern Iran. J Vector Borne Dis. 52: 63–72.
40. Nikookar SH, Fazeli-Dinan M, Azari-Ha-midian S, Mousavinasab SN, Arabi M, Ziapour SP, Shojaee J, Enayati A (2017) Species composition and abundance of mosquito larvae in relation with their hab-itat characteristics in Mazandaran Prov-ince, northern Iran. Bull Entomol Res. 107: 598–610.
41. Zaim M, Ershadi MRY, Manouchehri AV,
Hamdi MR (1986) The use of CDC light traps and other procedures for sampling malaria vectors in southern Iran. J Am Mosq Control Assoc. 2: 511–515.
42. Zaim M, Subbarao SK, Manouchehri AV, Cochrane AH (1993) Role of Anopheles culicifacies s.l. and An. pulcherrimus in malaria transmission in Ghassreghand (Baluchistan), Iran. J Am Mosq Control Assoc. 9: 23–26.
43. Zaim A, Manouchehri AV, Motabar M, Emadi AM, Nazari M, Pakdad K, Kayedi MH, Mowlaii G (1995) Anopheles cu-licifacies in Baluchistan, Iran. Med Vet Entomol. 9: 181–186.
44. Basseri H, Raeisi A, Ranjbar Khakha M, Pakarai A, Abdolghafar H (2010) Sea-sonal abundance and host-feeding pat-terns of anopheline vectors in malaria en-demic area of Iran. J Parasitol Res. 2010: 1–8.
45. Oshaghi MA, Vatandoost H, Gorouhi A, Abai MR, Madjidpour A, Arshi S, Sadeghi H, Nazari M, Mehravaran A (2011) Anopheline species composition in borderline of Iran-Azarbaijan. Acta Trop. 119: 44–49.
46. Maghsoodi N, Ladonni H, Basseri HR (2015) Species composition and seasonal activities of malaria vectors in an area at reintroduction prevention stage, Khuzestan, south-western Iran. J Arthro-pod-Borne Dis. 9: 60–70.
47. Sofizadeh A, Edalat H, Abai MR, Hanafi-Bojd AA (2016) Fauna and some bio-logical characteristics of Anopheles mos-quitoes (Diptera: Culicidae) in Kalaleh County, Golestan Province, northeast of Iran. Asia Pac J Trop Biomed. 6: 730–734.
48. Ghavami MB, Ladonni H (2006) The fauna and frequency of different mosquito spe-cies (Diptera: Culicidae) in Zanjan Prov-ince. J Zanjan Univ Med Sci. 13(53): 46–54 (in Persian with English abstract).
49. Navidpour S, Vazirianzadeh B, Harbach R,Jahanifard E, Moravvej SA (2012) The identification of culicine mosquitoes in the Shadegan wetland in southwestern Iran. J Insect Sci. 12: 1–6.
50. Soltani Z, Keshavarzi D, Ebrahimi M, Soltani A, Moemenbellah-Fard MJ, Soltani F, Faramarzi H, Amraee K, El-yasigomari A (2017) The fauna and ac-tive season of mosquitoes in west of Fars Province, southwest of Iran. Arch Razi Inst. 72: 203–208.
51. Reinert JF (2009) List of abbreviations for currently valid generic-level taxa in fam-ily Culicidae (Diptera). Eur Mosq Bull. 27: 68–76.
52. Tischler W (1949) Grundzüge der ter-restrischen Tierökologie. Friedrich Vieweg and Sohn Braunschweig.
53. Heydemann B (1955) Die Frage der topog-raphischen Übereinstimmung des Lebensraumes von Pflanzenund Tierge-sellschaften. Verh Dtsch Zool Ges Er-langen. 19: 444–452.
54. Gutsevich AV, Monchadskii AS, Shtakelberg AA (1974) Fauna of the USSR Diptera Volume III No4 Mosquitoes Family Culicidae. Akad Nauk SSSR Zo-ol Inst NS No 100, Leningrad (in Rus-sian, English translation by Lavoott R, edited by Theodor O, Israel Program for Scientific Translations, Jerusalem).
55. Shahhosseini N, Chinikar S (2016) Genetic evidence for circulation of Kunjinrelated West Nile virus strain in Iran. J Vector Borne Dis. 53: 384–386.
56. Pachler K, Lebl K, Berer D, Rudolf I, Hubálek Z, Nowotny N (2014) Putative new West Nile virus lineage in Urano-taenia unguiculata mosquitoes, Austria, 2013. Emerg Infect Dis. 20: 2119–2122.
57. Ludham KW, Jachowski LAJr, Otto GF (1970) Potential vectors of Dirofilaria immitis. J Am Vet Med Assoc. 157(10): 1354–1359.
58. Anderson RC (2000) Nematod Parasites of Vertebrates. Their Development and Transmission. 2nd ed. CABI Publishing, Wallingford.
59. Șuleșco T, von Thien H, Toderaș L, Toderaș I, Lühken R, Tannich E (2016) Circulation of Dirofilaria repens and Dirofilaria immitis in Moldova. Parasit Vector. 9(627): 1–11.
60. Azari-Hamidian S, Joeafshani MA, Moss-lem M, Rassaei AR (2003) Adult mos-quito habitats and resting-places in Guilan Province (Diptera: Culicidae). Hakim. 6: 55–62.
61. Alkan SS, Aldemir A (2010) Seasonal dynamics of mosquitoes (Diptera: Culicidae) in animal barns and houses in Aras Valley, Turkey. Kafkas Univ Vet Fak Derg. 16: 43–48.
62. Roiz D, Vasquez A, Rosa R, Munoz J, Arnoldi D, Rosso F, Fiuerola J, Tenorio A, Rizzoli A (2012) Blood meal analy-sis, flavivirus screening, and influence of meteorological variables on the dy-namics of potential mosquito vectors of West Nile virus in northern Italy. J Vect Ecol. 37: 20–28.
63. Alten B, Bellini R, Caglar SS, Simsek FM, Kaynas S (2000) Species composition and seasonal dynamics of mosquitoes in the Belek region of Turkey. J Vect Ecol. 25: 146–154.
64. Simsek FM (2004) Seasonal larval and adult population dynamics and breeding habitat diversity of Culex theileri The-obald, 1903 (Diptera: Culicidae) in the Golbasi District, Ankara, Turkey. Turk J Zool. 28: 337–344.
65. Alahmad AM (2012) Mosquito fauna (Diptera: Culicidae) of the eastern region of Saudi Arabia and their seasonal abun-dance. J King Saud Univ. 24: 55–62.
66. Ataie A, Moosa-Kazemi SH, Vatandoost H, Yaghoobi-Ershadi MR, Bakhshi H, Anjomruz M (2015) Assessing the sus-ceptibility status of mosquitoes (Diptera: Culicidae) in a dirofilariasis focus, north-western Iran. J Arthropod-Borne Dis. 9:7–21.
67. Ghorbani F, Vatandoost H, Hanafi-Bojd AA, Abai MR, Nikookar H, Enayati AA (2018) High resistance of vector of West Nile virus, Culex pipiens Linnaeus (Diptera: Culicidae) to different insecticides recommended by WHO in northern Iran. J Arthropod-Borne Dis. 12: 24–30.
How to Cite
Azari-Hamidian S, Norouzi B, Noorallahi A, Hanafi-Bojd AA. Seasonal Activity 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.
Original Article