Original Article

Population Fluctuations and Abundance Indices of Mosquitoes (Diptera: Culicid), as the Potential Bridge Vectors of Pathogens to Humans and Animals in Mazandaran Province, Northern Iran

Abstract

Background: Seasonal activity patterns of mosquitoes are essential as baseline knowledge to understand the transmis­sion dynamics of vector-borne diseases. This study was conducted to evaluate the monthly dynamics of the mosquito populations and their relation to meteorological factors in Mazandaran Province, north of Iran.Methods: Mosquito adults and larvae were collected from 16 counties of Mazandaran Province using different sam­pling techniques, once a month from May to December 2014. “Index of Species Abundance” (ISA) along with “Stand­ardized ISA” (SISA) was used for assessing the most abundant species of mosquitoes based on the explanations of Rob­ert and Hsi. Pearson’s correlation coefficient (R) was used to assess the relationships between the monthly population fluctuations and meteorological variables.Results: Overall, 23750 mosquitoes belonging to four genera and nineteen species were collected and identified. The highest population density of mosquitoes was in July and the lowest in May. The ISA/SISA indices for Culex pipiens were both 1 for larvae and 1.25/0.973 for adults in total catch performed in human dwellings. For Cx. tritaeniorhynchus, the ISA/SISA were 1.68/0.938 in pit shelter method. A significant positive correlation was observed between population fluctuations of Cx. tritaeniorhynchus and mean temperature (R: 0.766, P< 0.027).Conclusions: The results indicated that the mosquitoes are more active in July, and Cx. pipiens and Cx. tritaeniorhyn­chus were the most abundant species. Considering the potential of these species as vectors of numerous pathogens, con­trol programs can be planed based on their monthly activity pattern in the area.
1. Rueda LM (2008) Global diversity of mosquitoes (Insecta: Diptera: Culicidae) in freshwater. Hydrobiologia. 595: 477–487.
2. Gary R, Mullen and Lance A (2019) Mos-quitoes (Culicidae). In: Woodbridge A, Foster and Edward DW, Elsevier. pp. 261–325.
3. Suesdek L (2018) Microevolution of med-ically important mosquitoes–A review. Acta Trop. 191(2019): 162–171.
4. World Health Organization (2019) Global burden of major vector-borne diseases. Available at: https://www.who.int/vector-control/burden_vector-borne_diseases.pdf
5. World Health Organization (2020) World Malaria Report 2020. World Health Organization, Geneva, Switzerland.
6. Campos GS, Bandeira AC, Sardi SI (2015) Zika virus outbreak, bahia, brazil. Emerg Infect Dis. 21(10): 1885–1891.
7. Van Bortel W, Dorleans F, Rosine J, Blateau A, Rousset D, Matheus S, Leparc-Goffart I, Flusin O, Prat C, Cesaire R (2014) Chikungunya outbreak in the Caribbean region, December 2013 to March 2014, and the significance for Europe. Euro Surveill. 19(13): 20759.
8. Nash D, Mostashari F, Fine A, Miller J, O'leary D, Murray K, Huang A, Rosenberg A, Greenberg A, Sherman Ml (2001) The outbreak of West Nile virus infection in the New York City area in 1999. Engl J Med. 344(24): 1807–1814.
9. 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.
10. Nikookar SH, Fazeli-Dinan M, Azari-Hamidian S, Nasab SNM, Aarabi M, Ziapour SP (2018) Fauna, ecological characteristics, and checklist of the mosquitoes in Mazandaran Province, northern Iran. J Med Entomol. 55(3): 634–645.
11. Edrissian G (2006) Malaria in Iran: Past and present situation Iran J Parasitol. 1 (1): 1–14.
12. Zaim M, Subbarao S, Manouchehri A, Cochrane A (1993) Role of Anopheles culicifacies s.l. and An. pulcherrimus in malaria transmission in Ghassreghand (Baluchistan), Iran. J Am Mosq Control Assoc. 9(1): 23–26.
13. Sharifzadeh Y (2014) Species composition and some bionomic characters of Anopheles subpictus in Sarbaz District, south-eastern Iran. [PhD dissertation]. School of Public Health, Tehran University of Medical Sciences, Iran.
14. Dinparast Djadid N, Jazayeri H, Gholiza-deh S, Rad SP, Zakeri S (2009) First record of a new member of Anopheles Hyrcanus Group from Iran: molecular identification, diagnosis, phylogeny, status of kdr resistance and Plasmodium infection. J Med Entomol. 46(5): 1084–1093.
15. Hanafi-Bojd AA, Sedaghat MM, Vatandoost H, Azari-Hamidian S, Pakdad K (2018) Predicting environmentally suitable areas for Anopheles superpictus Grassi (s.l.), Anopheles maculipennis Meigen (s.l.) and Anopheles sacharovi Favre (Diptera: Culicidae) in Iran. Parasite Vectors. 11(1): 382–390.
16. Chinikar S, Ghiasi SM, Moradi M, Madihi SR (2010) Laboratory detection facility of Dengue fever (DF) in Iran: the first imported case. Int J Infect Dis. 8(1): 1–2.
17. Chinikar S, Ghiasi SM, Shah-Hosseini N, Mostafavi E, Moradi M, Khakifirouz S, Rasi Varai S, Rafigh M, Jalali T, Goya MM, Shirzadi MR, Zainali M, Fooks AR (2013) Preliminary study of dengue virus infection in Iran. Travel Med Infect Dis. 11(33): 166–169.
19. Pouriayevali MH, Rezaei F, Jalali T, Baniasadi V, Fazlalipour M, Mostafavi E, Khakifirou S, Mohammadi T, Fereydooni Z, Azad-Manjiri S, Hosseini M, Ghale-joogh M, Gouya MM, Failloux AB, Salehi- Vaziri M (2019) Imported cases of Chikungu¬nya virus in Iran. BMC Infect Dis. 19 (1): 1004.
18. Mardani M, Abbasi F, Aghahasani M, Ghavami B (2013) First Iranian imported case of dengue. Int J Prev Med. 4(9): 1075–1077.
20. Dow RP (1953) Notes on Iranian mosquitoes. Am J Trop Med Hyg. 2(4): 683–695.
21. Monchadskii AS (1951) The larvae of blood-sucking mosquitoes of the USSR and ad¬joining countries (Subfam-Culicinae). Opred Faune SSR Moscow. Zool. 37(1): 1–290.
22. Edwards FW (1921) A revision of the mosquitoes of the Palaearctic Region. Bull Entomol Res. 12(3): 263–351.
23. Doosti S, Yaghoobi-Ershadi MR, Schaffner F, Moosa-Kazemi SH, Akbarzadeh K, Gooya MM, Vatandoost H, Shirzadi MR, Mostafavi E (2016) Mosquito surveillance and the first record of the invasive mosquito species Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae) in southern Iran. Iran J Public Health. 45 (8): 1064–1073.
24. Sungvornyothin S, Kongmee M, Muenvorn V, Polsomboon S, Bangs MJ, Prabaripai A, Tantakom S, Chareonviriyaphap T (2009) Seasonal abundance and bloodfeeding activity of Anopheles dirus sensu lato in western Thailand. J Am Mosq Control Assoc. 25(4): 425–4231.
25. Bashar K, Tuno N (2014) Seasonal abundance of Anopheles mosquitoes and their association with meteorological factors and malaria incidence in Bangladesh. Parasite Vectors. 7(1): 442.
26. Rosa-Freitas MG, Tsouris P, Peterson AT, Honório NA, Barros FSMd, Aguiar DBd, Gurgel HdC, Arruda MEd, Vasconcelos SD, Luitgards-Moura JF (2007) An ecoregional classification for the state of Roraima, Brazil: the im-portance of landscape in malaria biology. Mem Inst Oswaldo Cruz. 102 (3): 349–358.
27. Loetti V, Burroni N, Vezzani D (2007) Seasonal and daily activity patterns of human-biting mosquitoes in a wetland system in Argentina. J Vector Ecol. 32 (2): 358–366.
28. Veronesi R, Gentile G, Carrieri M, Mac-cagnani B, Stermieri L, Bellini R (2012) Seasonal pattern of daily activity of Ae-des caspius, Aedes detritus, Culex mod-estus, and Culex pipiens in the Po Delta of northern Italy and significance for vector‐borne disease risk assessment. J Vector Ecol. 37(1): 49–61.
29. Alten B, Bellini R, Caglar S, Simsek F, Kaynas S (2000) Species composition and seasonal dynamics of mosquitoes in the Belek region of Turkey. J Vector Ecol. 25(2): 146–154.
30. Azari-Hamidian S, Norouzi B, Noorallahi A, Hanafi-Bojd AA (2018) 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.
31. Sofizadeh A, Edalat H, Abai MR, Hanafi-Bojd AA (2016) Fauna and some biological characteristics of Anopheles mosquitoes (Diptera: Culicidae) in Kalaleh County, Golestan Province, northeast of Iran. Asian Pac J Trop Biomed. 6(9): 730–734.
32. Sanei-Dehkordi A, Soleimani-Ahmadi M, Jaberhashemi SA, Zare M (2019) Spe-cies composition, seasonal abundance and distribution of potential anopheline vectors in a malaria endemic area of Iran: field assessment for malaria elimination. Malar J. 18(1): 157.
33. Nikookar S, Fazeli-Dinan M, Azari-Hamidian S, Mousavinasab S, Arabi M, Ziapour S, Shojaee J, Enayati A (2017) Species composition and abundance of mosquito larvae in relation with their habitat characteristics in Mazandaran Province, northern Iran. Bull Entomol Res. 107(5): 598–610.
34. Nikookar SH, Azari-Hamidian S, Fazeli-Dinan M, Nasab SNM, Aarabi M, Ziapour SP, Ahmadali AA (2016) Species composition, co-occurrence, association and affinity indices of mosquito larvae (Diptera: Culicidae) in Mazandaran Province, northern Iran. Acta Trop. 157: 20–29.
35. Nikookar SH, Moosa-Kazemi SH, Oshaghi MA, Vatandoost H, Yaghoobi-Ershadi MR, Enayati AA, Motevali-Haghi F, Zia¬pour SP, Fazeli-Dinan M (2015) Biodiversity of culicid mosquitoes in rural Neka township of Mazandaran Province, northern Iran. J Vector Borne Dis. 52 (1): 63–72.
36. Azari-Hamidian S (2007) Checklist of Iranian mosquitoes (Diptera: Culicidae). J Vector Ecol. 32(2): 235–242.
37. Reinert JF (2009) List of abbreviations for currently valid generic-level taxa in fam-ily Culicidae (Diptera). Eurp Mosq Bull. 27: 68–76.
38. Roberts D, Hsi B (1979) An index of species abundance for use with mosquito surveillance data. Environ Entomol. 8(6): 1007–1013.
39. Silva JdS, Souto Couri M, de Leão Giupponi AP, Alencar J (2014) Mosquito fauna of the Guapiaçu Ecological Reserve, Cachoeiras de Macacu, Rio de Janeiro, Brazil, collected under the influence of different color CDC light traps. J Vector Ecol. 39(2): 384–394.
40. Bolling BG, Barker CM, Moore CG, Pape WJ, Eisen L (2009) Seasonal patterns for entomological measures of risk for exposure to Culex vectors and West Nile virus in relation to human disease cases in northeastern Colorado. J Med Entomol. 46(6): 1519–1531.
41. Gutiérrez-Bugallo G, Piedra LA, Rodriguez M, Bisset JA, Lourenço-de-Oliveira R, Weaver SC, Vasilakis N, Vega-Rúa A (2019) Vector-borne transmission and evolution of Zika virus. Nat Ecol Evol. 3(4): 561–569.
42. Nikookar SH, Moosa-Kazemi SH, Oshaghi M, Yaghoobi-Ershadi M, Vatandoost H, Kianinasab A (2010) Species composition and diversity of mosquitoes in Neka County, Mazandaran Province, northern Iran. Iran J Arthropod Borne Dis. 4(2): 26–34.
43. Nikookar SH, Moosa-Kazemi SH, Yaghoobi-Ershadi MR, Vatandoost H, Oshaghi MA, Ataei A, Anjamrooz M (2015) Fauna and larval habitat characteristics of mosquitoes in Neka County, northern Iran. J Arthropod Borne Dis. 9(2): 253–266.
44. Azari-Hamidian S (2007) Larval habitat characteristics of mosquitoes of the genus Culex (Diptera: Culicidae) in Guilan Province, Iran. Iran J Arthropod Borne Dis. 1(1): 9–20.
45. Khoshdel-Nezamiha F, Vatandoost H, Azari-Hamidian S, Mohammadi-Bavani M, Dabiri F, Entezar-Mahdi R, Chavshin AR (2014) Fauna and larval habitats of mosquitoes (Diptera: Culicidae) of West Azerbaijan Province, Northwestern Iran. J Arthropod Borne Dis. 8(2): 163–73.
46. Gorsich EE, Beechler BR, van Bodegom PM, Govender D, Guarido MM, Venter M, Schrama M (2019) A comparative assessment of adult mosquito trapping methods to estimate spatial patterns of abundance and community composition in southern Africa. Parasit Vector. 12(1): 462.
47. Gunduz YK, Aldemir A, Alten B (2009) Seasonal dynamics and nocturnal activities of mosquitoes (Diptera: Culicidae) in Aras Valley, Turkey. Turk J Zool. 33: 269–276.
48. Alten B, Caglar S, Özer N (2000) Malaria and its vectors in Turkey. Eur Mosq bull. 7: 27–33.
49. Bogojević MS, Merdić E, Turić N, Jeličić Ž, Zahirović Ž, Vrućina I, Merdić S (2009) Seasonal dynamics of mosquitoes (Diptera: Culicidae) in Osijek (Croatia) for the period 1995–2004. Biologia. 64 (4): 760–767.
50. Roiz D, Vazquez A, Rosà R, Muñoz J, Arnoldi D, Rosso F, Figuerola J, Tenorio A, Rizzoli A (2012) Blood meal analysis, flavivirus screening, and influence of meteorological variables on the dynamics of potential mosquito vectors of West Nile virus in northern Italy. J Vector Ecol. 37(1): 20–28.
51. Fritz M, Walker E, Miller J, Severson D, Dworkin I (2015) Divergent host preferences of above‐and below‐ground Culex pipiens mosquitoes and their hybrid off-spring. Med Vet Entomol. 29(2): 115–123.
52. Farajollahi A, Fonseca DM, Kramer LD, Kilpatrick AM (2011) “Bird biting” mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect Genet Evol. 11(7): 1577–1585.
53. 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 Int Health. 22(10): 1343–1349.
54. Das BP (2012) Mosquito Vectors of Japanese Encephalitis Virus from Northern India: Role of BPD Hop Cage Method: Springer New Dehli Heidelberg New York Dorderechet, Londan.
55. 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(105): 1–6.
56. Lytra I, Emmanouel N (2014) Study of Culex tritaeniorhynchus and species com¬position of mosquitoes in a rice field in Greece. Acta Trop. 134: 66–71.
57. Miller BR, Godsey MS, Crabtree MB, Savage HM, Al-Mazrao Y, Al-Jeffri MH, Abdoon MM, Al-Seghayer SM, Al-Shahrani AM, Ksiazek TG (2002) Isolation and genetic characterization of Rift Valley fever virus from Aedes vexans ara¬biensis, Kingdom of Saudi Arabia. Emerg Infect Dis .8(12): 1492–1494.
58. Harbach RE (1988) The mosquitoes of the subgenus Culex in southwestern Asia and Egypt (Diptera: Culicidae). Contrib Amer Ent Inst. 24(1): 1–237.
59. Abai M, Azari-Hamidian S, Ladonni H, Hakimi M, Mashhadi-Esmail K, Sheikhzadeh K, Kousha M, Vatan¬doost H (2007) Fauna and checklist of mosquitoes (Diptera: Culicidae) of East Azerbaijan Province, northwestern Iran. Iran J Arthropod Borne Dis. 1(2): 27–33.
60. 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(1): 37–53.
61. Aldemir A, Bosgelmez A (2006) Popula-tion dynamics of adults and immature stages of mosquitoes (Diptera: Culicidae) in Gölbaşı District, Ankara. Turk J Zool. 30(1): 9–17.
62. Sedaghat MM, Linton YM, Oshaghi MA, Vatandoost H, Harbach RE (2004) The Anopheles maculipennis complex (Diptera: Culicidae) in Iran: molecular characterization and recognition of a new species. Bull Entomol Res. 93(6): 527–536.
63. Hubálek Z, Halouzka J (1999) West Nile fever--a reemerging mosquito-borne viral disease in Europe. Emerg Infect Dis. 5(5): 643–650.
64. Pachler K, Lebl K, Berer D, Rudolf I, Hubalek Z, Nowotny N (2014) Putative new West Nile virus lineage in Uranotaenia unguiculata mosquitoes, Austria, 2013. Emerg Infect Dis. 20(12): 2119.
65. Nanfack Minkeu F, Vernick KD (2018) A systematic review of the natural virome of Anopheles mosquitoes. Viruses. 10(5): 222.
66. Naficy K, Saidi S (1970) Serological survey on viral antibodies in Iran. Trop Ge-ogr Med. 22(2): 183–188.
67. Alkan SS, Aldemir A (2010) Seasonal dynamics of mosquitoes (Diptera: Cu-licidae) in animal barns and houses in Aras Valley, Turkey. Kafkas Univ Vet Fak Derg. 16(1): 43–48.
68. Aldemir A, Demirci B, Kirpik MA, Alten B, Baysal A (2009) Species composition and seasonal dynamics of mosquito larvae (Diptera: Culicidae) in Iğdır Plain, Tur¬key. Kafkas Univ Vet Fak Derg. 15: 103–110.
69. Hu W, Tong S, Mengersen K, Oldenburg B (2006) Rainfall, mosquito density and the transmission of Ross River virus: A time-series forecasting model. Ecol Modell. 196(3–4): 505–514.
70. Medlock J, Snow K, Leach S (2005) Po-tential transmission of West Nile virus in the British Isles: an ecological review of candidate mosquito bridge vectors. Med Vet Entomol 19(1): 2–21.
71. Zeller H, Schuffenecker I (2004) West Nile virus: an overview of its spread in Europe and the Mediterranean basin in contrast to its spread in the Americas. Eur J Clin Microbiol Infect Dis. 23(3): 147–156.
72. Azari Hamidian S, Joeafshani MA, Moss-lem M, Rassaei AR (2003) Adult mos-quito habitats and resting-places in Guilan Province (Diptera: Culicidae). Hakim Res J. 6(3): 55–62 (In Persian with English abstract).
73. Moosa-Kazemi S, Vatandoost H, Ni-kookar H, Fathian M (2009) Culicinae (Diptera: culicidae) mosquitoes in Chabahar County, Sistan and Baluchistan Province, southeastern Iran. Iran J Arthropod Borne Dis. 3(1): 29–35.
74. Nikookar SH, Fazeli-Dinan M, Enayati A, Zaim M (2020) Zika; a continuous global threat to public health. Environ Res. 188: 109868.
75. L'Ambert G, Ferré JB, Schaffner F, Fon-tenille D (2012) Comparison of different trapping methods for surveillance of mosquito vectors of West Nile virus in Rhône Delta, France. J Vector Ecol. 37(2): 269–275.
76. Lundström JO (1999) Mosquito-borne viruses in western Europe: a review. J Vector Ecol. 24(1): 1–39.
77. Rudolf I, Sebesta O, Mendel J, Betasova L, Bockova E, Jedlickova P, Venclikova K, Blazejova H, Sikutova S, Hubalek Z (2014) Zoonotic Dirofilaria repens (Nematoda: Filarioidea) in Aedes vexans mosquitoes, Czech Republic. Parasitol Res. 113(12): 4663–4667.
78. Elizondo-Quiroga D, Medina-Sánchez A, Sánchez-González JM, Eckert KA, Vil-lalobos-Sánchez E, Navarro-Zúñiga AR, Sánchez-Tejeda G, Correa-Morales F, González-Acosta C, Arias FC (2018) Zika virus in salivary glands of five different species of wild-caught mosquitoes from Mexico. Sci Rep. 8(1): 1–7.
79. Benedum CM, Seidahmed OM, Eltahir EA, Markuzon N (2018) Statistical modeling of the effect of rainfall flushing on dengue transmission in Singapore. PLOS Negl Trop Dis. 12(12): e0006935.
80. Talla C, Diallo D, Dia I, Ba Y, Ndione JA, Morse A, Diop A, Diallo M (2014) Statistical modeling of the abundance of vectors of West African Rift Valley fever in Barkédji, Senegal. PLoS One. 9 (12): e114047.
81. Chuang TW, Hildreth MB, Vanroekel DL, Wimberly MC (2011) Weather and land cover influences on mosquito populations in Sioux Falls, South Dakota. J Med Entomol. 48(3): 669–679.
82. Diallo D, Talla C, Ba Y, Dia I, Sall AA, Diallo M (2011) Temporal distribution and spatial pattern of abundance of the Rift Valley fever and West Nile fever vectors in Barkedji, Senegal. J Vector Ecol. 36(2): 426–436.
83. Janousek T, Kramer aL (1999) Seasonal incidence and geographical variation of Ne¬braska mosquitoes, 1994–95. J Am Mosq Control Assoc.15(3): 253–262.
Files
IssueVol 15 No 2 (2021) QRcode
SectionOriginal Article
DOI https://doi.org/10.18502/jad.v15i2.7490
Keywords
Seasonal activity; Mosquitoes; Abundance indices; Mazandaran; Caspian Sea littoral

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Nikookar SH, Fazeli-Dinan M, Enayati A. Population Fluctuations and Abundance Indices of Mosquitoes (Diptera: Culicid), as the Potential Bridge Vectors of Pathogens to Humans and Animals in Mazandaran Province, Northern Iran. J Arthropod Borne Dis. 2022;15(2):207-224.