Predicting the Distribution of Culex pipiens (Diptera: Culicidae) in Golestan Province of Iran using an Ecological Niche Model
,
Abstract
Background: Culex pipiens is one of the most important vectors of mosquito-borne pathogens in Iran. This study aimed to predict the distribution of this species in Golestan Province, Iran, and to determine the factors affecting its distribution.
Methods: Mosquito larvae were collected by using the dipping method from 56 locations across all 14 counties of the province, between April and October 2016. Species were identified morphologically, and the spatial distribution of Cx. pipiens was modeled using the maximum entropy (MaxEnt software Ver. 3.3.3) model.
Results: The results of our study show that areas located in the central part of Golestan Province are the most environmentally suitable habitat for Cx. pipiens. Jackknife test of variable importance showed that the following factors had the greatest influence on the distribution of Cx. pipiens: proximity to human settlements, precipitation of coldest quarter (mm), precipitation of wettest quarter (mm), precipitation of wettest month (mm), and mean temperature of coldest quarter (oC).
Conclusion: This study concludes that the MaxEnt model is a very suitable model for studying the ecology of Cx. pipiens and precipitation, and temperature play a major role in the distribution of this species.
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2. Marcolin L, Zardini A, Longo E, Caputo B, Poletti P, Marco MD (2025) Mapping the habitat suitability of Culex pipiens in Eu¬rope using ensemble bioclimatic mod-elling. bioRxiv. 52 (10): 1–11.
3. Abdallah FI, Merdan BA, Shaarawi FA, Mo¬hamed AF, Selim TA, Dahesh SM, Rady MH (2024) The potentiality of Culex pipiens (Diptera: Culicidae) complex holobiont in transmitting the hepatitis C virus (HCV) with the aid of bacterial microbiota in the midgut. Beni-Suef Univ J Basic Appl Sci. 13 (119): 1–10.
4. Koosha M, Oshaghi MA, Sedaghat MM, Vatan¬doost H, Azari-Hamidian S, Abai MR, Hanafi-Bojd AA, Mohtarami F (2017) Se¬quence analysis of mtDNA COI barcode region revealed three haplotypes within Cu¬lex pipiens assemblage. Exp Parasitol. 181: 102–110.
5. Dehghan H, Sadraei J, Moosa-Kazemi SH (2010) The Morphological variations of Cu¬lex pipiens larvae (Diptera: Culicidae) in Yazd Province, Central Iran. Iran J Ar-thropod-Borne Dis. 4(2): 42–49.
6. Karami M, Moosa-Kazemi SH, Oshaghi MA, Vatandoost H, Sedaghat MM, Ra-jabnia R, Hosseini M, Maleki-Ravasan N, Yahya¬pour Y, Ferdosi-Shahandashti E (2016) Wolbach¬ia Endobacteria in natural populations of Culex pipiens of Iran and its phylogenetic congruence. J Arthro¬pod-Borne Dis. 10 (3): 347–63.
7. Azari-Hamidian S, Joeafshani MA, Moss-lem M, Rassaei AR (2005) Mosquito fauna and distribution of the genus Culex (Diptera: Culicidae) in Guilan Province. J Pajou-hesh and Sazandegi. 68: 39–45 (Persian).
8. Sofizadeh A, Moosa-Kazemi SH, Dehghan H (2017) Larval habitats characteristics of mosquitoes (Diptera: Culicidae) in north-east of Iran. J Arthropod-Borne Dis. 11 (2):211–225.
9. 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 char-acteristics of mosquitoes (Diptera: Cu-licidae) in Golestan Province, Northeast of Iran, 2014–2015. J Arthropod-Borne Dis. 12(3): 240–251.
10. Hassan MM, Al-Atawi NDAA, Medadi Kaabi MAM, Eid Alatawi SS, Harban Haider NA, Mohammed Al-Atawi AA (2020) Characterization and distribution of larval habitats of Culex pipiens complex (Diptera: Culicidae) vec-tors of West Nile Virus in Tabuk town, Saudi Arabia. Int J Mosq Res. 7(5): 60–68.
11. Mousakazemi S, Zaim M, Zahraii A (2000) Fauna and ecology of Culicidae of the Zar¬rin-Shahr and Mobarakeh area in Isfahan Province. Armaghan Danesh, J Yasuj Uni Med Sci. 5: 46–54 (Persian).
12. Nikookar SH, Fazeli-Dinan M, Azari-Ha-midian S, Mousavinasab SN, Arabi M, Zia¬pour SP, Shojaee J, Enayati A (2017) Spe¬cies composition and abundance of mos¬quito larvae in relation with their habitat characteristics in Mazandaran Province, northern Iran. J Bull Entomol Res. 107(5): 598–610.
13. Larson SR, DeGroote JP (2010) Ecologi-cal niche modeling of potential West Nile virus vector mosquito species in Iowa. J Insect Sci. 10(110): 1–17.
14. Mweya CN, Kimera SI, Kija JB, Leonard E, Mboera G (2013) Predicting distribu-tion of Aedes aegypti and Culex pipiens com¬plex, potential vectors of Rift Valley fever vi¬rus in relation to disease epidem-ics in East Africa. Infect Ecol Epidemiol. 3(1): 1–7.
15. Ragab SH, Alkhaibari AM, Alharbi J, Areshi SM, Mashlawi AM, Embaby DM, Tyshen¬ko MG, Selim TA, Kamel M (2025) Impact of climate change on Culex pipiens mos¬quito distribution in the United States. Sustainability. 17(1): 1–18.
16. Conley AK, Fuller DO, Haddad N, Has-san AN, Gad AM, Beier JC (2014) Mod-eling the distribution of the West Nile and Rift Valley Fever vector Culex pipiens in arid and semi-arid regions of the Middle East and North Africa. Parasit Vectors. 7: 289.
17. Mughnini-Gras L, Mulatti P, Severini F, Boccolini D, Romi R, Bongiorno G, Khoury C, Bianchi R, Montarsi F, Patregnani T, Bonfanti L, Rezza G, Ca-pelli G, Busani L (2014) Ecological niche modelling of po¬tential West Nile Virus vector mosquito species and their geo-graphical association with equine epizo-otics in Italy. Eco Health. 11: 120–132.
18. Adham D, Moradi-Asl E, Vatandoost H, Saghafipour A (2019) Ecological niche modeling of West Nile virus vector in Northwest of Iran. Oman Med J. 34(6): 514–520.
19. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of spe¬cies geographic distributions. J Ecol Model. 190: 231–259.
20. Elith J, Graham CH, Anderson RP, Dud Ferrier MS, Guisan A, Hijmans RJ, Huett-mann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G (2006) Novel methods improve predic¬tion of species distributions from occur¬rence da¬ta. J Ecography. 29: 129–151.
21. Golfiruzi S, Kourdi Kh, Abolhasani M (2012) Statistics Yearbook of Health cen-ter in Golestan Province (2010–2011). Vol. 1. Noroozi Press, Gorgan, Iran, pp. 6–92 (Persian).
22. 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.
23. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high res¬olution interpolated climate surfaces for global land areas. Int J Climatol. 25: 1965–1978.
24. World-Clim (2016) Global Climate Data. University of California, Berkeley, Cali-fornia, USA. Available at: http://www.worldclim.org.
25. Phillips S, Dudek M, Schapire R (2004) A maximum entropy approach to species distribution modeling. The 21st Interna-tional Conference on Machine Learning. 2004 July 4–8, ACML, Banff, Canada, pp. 655–662.
26. Doosti S, Yaghoobi-Ershadi MR, Seda-ghat MM, Akbarzadeh K (2021) Larval habi¬tats characteristics of Culicinae sub-family in the south of Iran. Nusantara Bi-osci. 13 (2): 194–201.
27. Beji M, Rhim A, Roiz D, Bouattour A (2017) Ecophysiological characterization and molecular differentiation of Culex pipiens forms (Diptera: Culicidae) in Tu-nisia. Parasit Vectors. 10(1): 327.
28. Gonzalez C, Wang O, Strutz SE, Gonza-lez-Salazar C, Sanchez-Cordero V, Sarker S (2010) Climate change and risk of leish-maniasis in North America: pre¬dictions from ecological niche models of vector and res¬ervoir species. PLoS Negl Trop Dis. 4(1): e585.
29. Kronenwetter-Koepel TA, Meece JK, Miller CA, Reed KD (2005) Surveillance of above and below-ground mosquito breeding hab¬itats in a rural Midwestern community: Base¬line data for larvicidal control measures against West Nile virus vectors. Clin Med Res. 3(1): 3–12.
30. Joens CE, Lounibos LP, Marra PP, Kil-patrick AM (2012) Rainfall influences sur¬vival of Cx. pipiens (Diptera: Cu-licidae) in a residential neighborhood in the mid-Atlan¬tic USA. J Med Entomol. 49(3): 467–473.
31. Tran A, Gardon J, Weber S, Polidori L (2002) Mapping disease incidence in sub-urban areas using remotely sensed da¬ta. Am J Epidemiol. 156(7): 662–668.
32. Andreadis TG, Anderson JF, Vossbrinck CR, Main AJ (2004) Epidemiology of West Nile virus in Connecticut: a five-year anal¬ysis of mosquito data 1999-2003. Vector Borne Zoonotic Dis. 4(4): 360–378.
33. Lebl K, Brugger K, Rubel F (2013) Pre-dicting Culex pipiens/restuans population dynamics by interval lagged weather da-ta. Parasit Vectors. 6: 129.
34. Wang JN, Ogden H, Zhu H (2011) The impact of weather conditions on Culex pipiens and Culex restuans (Diptera: Cu-licidae) abundance: a case study in Peel region. J Med Entomol. 48(2): 468–475.
35. Chuang TW, Ionides EL, Knepper RG, Stanuszek WW, Walker ED, Wilson ML (2012) Cross-correlation map analyses show weather variation influences on mosquito abundance patterns in Saginaw County, Mich¬igan, 1989–2005. J Med Entomol. 49 (4): 851–858.
36. Rosa R, Marini G, Bolzoni L, Neteler M, Metz M, Delucchi L, Chadwick EA, Bal-bo L, Mosca A, Giacobini M, Bertolotti L, Rizzoli A (2014) Early warning of West Nile virus mosquito vector: climate and land use models successfully explain phenolo¬gy and abundance of Culex pipiens mos¬quitoes in north-western Ita¬ly. Parasit Vec¬tors. 7: 269.
37. Ippoliti C, Bonicelli L, De Ascentis M, Tora S, Di Lorenzo A, d’Alessio SG, Por-rello A, Bonanni A, Cioci D, Goffredo M, Calderara S, Conte A (2024) Spotting Culex pipiens from satellite: modeling hab¬itat suitability in central Italy using Senti¬nel-2 and deep learning techniques. Front Vet Sci. 11: 1383320.
38. Koenraadt CJ, Harrington LC (2008) Flush¬ing effect of rain on container-inhabiting mosquitoes Aedes aegypti and Culex pipiens (Diptera: Culicidae). J Med Ento¬mol. 45 (1): 28–35.
39. Di Pol G, Crotta M, Taylor RA (2022) Modelling the temperature suitability for the risk of West Nile Virus establishment in European Culex pipiens populations. Transbound Emerg Dis. 69(5): 1787–1799.
40. Abbasi M, Oshaghi MA, Sedaghat MM, Hazratian T, Rahimi Foroushani A, Jafa¬ri-Koshki T, Reza Yaghoobi-Ershadi M, Reza Abai M, Vatandoost H, Fekri Jaski S, Bozorg Omid F, Hanafi-Bojd AA (2023) Development of a degree-day model to pre¬dict the growth of Anopheles stephensi (Diptera: Culicidae): implica¬tion for vec¬tor control management. En¬viron Ento¬mol. 52(6): 1126–1138.
41. Kiarie-Makara MW, Ngumbi PM, Lee DK (2015) Effects of temperature on the growth and development of Culex pipiens com¬plex mosquitoes (Diptera: Culicidae). IOSR-JPBS. 10(6): 1–10.
42. Yoo EH, Chen D, Diao C, Russell C (2016) The effects of weather and envi-ronmental factors on West Nile virus mosquito abun¬dance in Greater Toronto Area. J Earth Interact. 20(3): 1–22.
2. Marcolin L, Zardini A, Longo E, Caputo B, Poletti P, Marco MD (2025) Mapping the habitat suitability of Culex pipiens in Eu¬rope using ensemble bioclimatic mod-elling. bioRxiv. 52 (10): 1–11.
3. Abdallah FI, Merdan BA, Shaarawi FA, Mo¬hamed AF, Selim TA, Dahesh SM, Rady MH (2024) The potentiality of Culex pipiens (Diptera: Culicidae) complex holobiont in transmitting the hepatitis C virus (HCV) with the aid of bacterial microbiota in the midgut. Beni-Suef Univ J Basic Appl Sci. 13 (119): 1–10.
4. Koosha M, Oshaghi MA, Sedaghat MM, Vatan¬doost H, Azari-Hamidian S, Abai MR, Hanafi-Bojd AA, Mohtarami F (2017) Se¬quence analysis of mtDNA COI barcode region revealed three haplotypes within Cu¬lex pipiens assemblage. Exp Parasitol. 181: 102–110.
5. Dehghan H, Sadraei J, Moosa-Kazemi SH (2010) The Morphological variations of Cu¬lex pipiens larvae (Diptera: Culicidae) in Yazd Province, Central Iran. Iran J Ar-thropod-Borne Dis. 4(2): 42–49.
6. Karami M, Moosa-Kazemi SH, Oshaghi MA, Vatandoost H, Sedaghat MM, Ra-jabnia R, Hosseini M, Maleki-Ravasan N, Yahya¬pour Y, Ferdosi-Shahandashti E (2016) Wolbach¬ia Endobacteria in natural populations of Culex pipiens of Iran and its phylogenetic congruence. J Arthro¬pod-Borne Dis. 10 (3): 347–63.
7. Azari-Hamidian S, Joeafshani MA, Moss-lem M, Rassaei AR (2005) Mosquito fauna and distribution of the genus Culex (Diptera: Culicidae) in Guilan Province. J Pajou-hesh and Sazandegi. 68: 39–45 (Persian).
8. Sofizadeh A, Moosa-Kazemi SH, Dehghan H (2017) Larval habitats characteristics of mosquitoes (Diptera: Culicidae) in north-east of Iran. J Arthropod-Borne Dis. 11 (2):211–225.
9. 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 char-acteristics of mosquitoes (Diptera: Cu-licidae) in Golestan Province, Northeast of Iran, 2014–2015. J Arthropod-Borne Dis. 12(3): 240–251.
10. Hassan MM, Al-Atawi NDAA, Medadi Kaabi MAM, Eid Alatawi SS, Harban Haider NA, Mohammed Al-Atawi AA (2020) Characterization and distribution of larval habitats of Culex pipiens complex (Diptera: Culicidae) vec-tors of West Nile Virus in Tabuk town, Saudi Arabia. Int J Mosq Res. 7(5): 60–68.
11. Mousakazemi S, Zaim M, Zahraii A (2000) Fauna and ecology of Culicidae of the Zar¬rin-Shahr and Mobarakeh area in Isfahan Province. Armaghan Danesh, J Yasuj Uni Med Sci. 5: 46–54 (Persian).
12. Nikookar SH, Fazeli-Dinan M, Azari-Ha-midian S, Mousavinasab SN, Arabi M, Zia¬pour SP, Shojaee J, Enayati A (2017) Spe¬cies composition and abundance of mos¬quito larvae in relation with their habitat characteristics in Mazandaran Province, northern Iran. J Bull Entomol Res. 107(5): 598–610.
13. Larson SR, DeGroote JP (2010) Ecologi-cal niche modeling of potential West Nile virus vector mosquito species in Iowa. J Insect Sci. 10(110): 1–17.
14. Mweya CN, Kimera SI, Kija JB, Leonard E, Mboera G (2013) Predicting distribu-tion of Aedes aegypti and Culex pipiens com¬plex, potential vectors of Rift Valley fever vi¬rus in relation to disease epidem-ics in East Africa. Infect Ecol Epidemiol. 3(1): 1–7.
15. Ragab SH, Alkhaibari AM, Alharbi J, Areshi SM, Mashlawi AM, Embaby DM, Tyshen¬ko MG, Selim TA, Kamel M (2025) Impact of climate change on Culex pipiens mos¬quito distribution in the United States. Sustainability. 17(1): 1–18.
16. Conley AK, Fuller DO, Haddad N, Has-san AN, Gad AM, Beier JC (2014) Mod-eling the distribution of the West Nile and Rift Valley Fever vector Culex pipiens in arid and semi-arid regions of the Middle East and North Africa. Parasit Vectors. 7: 289.
17. Mughnini-Gras L, Mulatti P, Severini F, Boccolini D, Romi R, Bongiorno G, Khoury C, Bianchi R, Montarsi F, Patregnani T, Bonfanti L, Rezza G, Ca-pelli G, Busani L (2014) Ecological niche modelling of po¬tential West Nile Virus vector mosquito species and their geo-graphical association with equine epizo-otics in Italy. Eco Health. 11: 120–132.
18. Adham D, Moradi-Asl E, Vatandoost H, Saghafipour A (2019) Ecological niche modeling of West Nile virus vector in Northwest of Iran. Oman Med J. 34(6): 514–520.
19. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of spe¬cies geographic distributions. J Ecol Model. 190: 231–259.
20. Elith J, Graham CH, Anderson RP, Dud Ferrier MS, Guisan A, Hijmans RJ, Huett-mann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G (2006) Novel methods improve predic¬tion of species distributions from occur¬rence da¬ta. J Ecography. 29: 129–151.
21. Golfiruzi S, Kourdi Kh, Abolhasani M (2012) Statistics Yearbook of Health cen-ter in Golestan Province (2010–2011). Vol. 1. Noroozi Press, Gorgan, Iran, pp. 6–92 (Persian).
22. 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.
23. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high res¬olution interpolated climate surfaces for global land areas. Int J Climatol. 25: 1965–1978.
24. World-Clim (2016) Global Climate Data. University of California, Berkeley, Cali-fornia, USA. Available at: http://www.worldclim.org.
25. Phillips S, Dudek M, Schapire R (2004) A maximum entropy approach to species distribution modeling. The 21st Interna-tional Conference on Machine Learning. 2004 July 4–8, ACML, Banff, Canada, pp. 655–662.
26. Doosti S, Yaghoobi-Ershadi MR, Seda-ghat MM, Akbarzadeh K (2021) Larval habi¬tats characteristics of Culicinae sub-family in the south of Iran. Nusantara Bi-osci. 13 (2): 194–201.
27. Beji M, Rhim A, Roiz D, Bouattour A (2017) Ecophysiological characterization and molecular differentiation of Culex pipiens forms (Diptera: Culicidae) in Tu-nisia. Parasit Vectors. 10(1): 327.
28. Gonzalez C, Wang O, Strutz SE, Gonza-lez-Salazar C, Sanchez-Cordero V, Sarker S (2010) Climate change and risk of leish-maniasis in North America: pre¬dictions from ecological niche models of vector and res¬ervoir species. PLoS Negl Trop Dis. 4(1): e585.
29. Kronenwetter-Koepel TA, Meece JK, Miller CA, Reed KD (2005) Surveillance of above and below-ground mosquito breeding hab¬itats in a rural Midwestern community: Base¬line data for larvicidal control measures against West Nile virus vectors. Clin Med Res. 3(1): 3–12.
30. Joens CE, Lounibos LP, Marra PP, Kil-patrick AM (2012) Rainfall influences sur¬vival of Cx. pipiens (Diptera: Cu-licidae) in a residential neighborhood in the mid-Atlan¬tic USA. J Med Entomol. 49(3): 467–473.
31. Tran A, Gardon J, Weber S, Polidori L (2002) Mapping disease incidence in sub-urban areas using remotely sensed da¬ta. Am J Epidemiol. 156(7): 662–668.
32. Andreadis TG, Anderson JF, Vossbrinck CR, Main AJ (2004) Epidemiology of West Nile virus in Connecticut: a five-year anal¬ysis of mosquito data 1999-2003. Vector Borne Zoonotic Dis. 4(4): 360–378.
33. Lebl K, Brugger K, Rubel F (2013) Pre-dicting Culex pipiens/restuans population dynamics by interval lagged weather da-ta. Parasit Vectors. 6: 129.
34. Wang JN, Ogden H, Zhu H (2011) The impact of weather conditions on Culex pipiens and Culex restuans (Diptera: Cu-licidae) abundance: a case study in Peel region. J Med Entomol. 48(2): 468–475.
35. Chuang TW, Ionides EL, Knepper RG, Stanuszek WW, Walker ED, Wilson ML (2012) Cross-correlation map analyses show weather variation influences on mosquito abundance patterns in Saginaw County, Mich¬igan, 1989–2005. J Med Entomol. 49 (4): 851–858.
36. Rosa R, Marini G, Bolzoni L, Neteler M, Metz M, Delucchi L, Chadwick EA, Bal-bo L, Mosca A, Giacobini M, Bertolotti L, Rizzoli A (2014) Early warning of West Nile virus mosquito vector: climate and land use models successfully explain phenolo¬gy and abundance of Culex pipiens mos¬quitoes in north-western Ita¬ly. Parasit Vec¬tors. 7: 269.
37. Ippoliti C, Bonicelli L, De Ascentis M, Tora S, Di Lorenzo A, d’Alessio SG, Por-rello A, Bonanni A, Cioci D, Goffredo M, Calderara S, Conte A (2024) Spotting Culex pipiens from satellite: modeling hab¬itat suitability in central Italy using Senti¬nel-2 and deep learning techniques. Front Vet Sci. 11: 1383320.
38. Koenraadt CJ, Harrington LC (2008) Flush¬ing effect of rain on container-inhabiting mosquitoes Aedes aegypti and Culex pipiens (Diptera: Culicidae). J Med Ento¬mol. 45 (1): 28–35.
39. Di Pol G, Crotta M, Taylor RA (2022) Modelling the temperature suitability for the risk of West Nile Virus establishment in European Culex pipiens populations. Transbound Emerg Dis. 69(5): 1787–1799.
40. Abbasi M, Oshaghi MA, Sedaghat MM, Hazratian T, Rahimi Foroushani A, Jafa¬ri-Koshki T, Reza Yaghoobi-Ershadi M, Reza Abai M, Vatandoost H, Fekri Jaski S, Bozorg Omid F, Hanafi-Bojd AA (2023) Development of a degree-day model to pre¬dict the growth of Anopheles stephensi (Diptera: Culicidae): implica¬tion for vec¬tor control management. En¬viron Ento¬mol. 52(6): 1126–1138.
41. Kiarie-Makara MW, Ngumbi PM, Lee DK (2015) Effects of temperature on the growth and development of Culex pipiens com¬plex mosquitoes (Diptera: Culicidae). IOSR-JPBS. 10(6): 1–10.
42. Yoo EH, Chen D, Diao C, Russell C (2016) The effects of weather and envi-ronmental factors on West Nile virus mosquito abun¬dance in Greater Toronto Area. J Earth Interact. 20(3): 1–22.
| Files | ||
| Issue | Vol 19 No 2 (2025) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v19i2.20191 | |
| Keywords | ||
| House mosquito Culex pipiens Ecological niche modeling Maximum entropy | ||
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How to Cite
1.
Kalteh EA, Yatimparvar G, Sofizadeh A, Sahneh E. Predicting the Distribution of Culex pipiens (Diptera: Culicidae) in Golestan Province of Iran using an Ecological Niche Model. J Arthropod Borne Dis. 2025;19(2):125-137.
