J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche …

Original Article Using Ecological Niche Modeling to Predict the Spatial Distribution of Anopheles maculipennis s.l. and Culex theileri (Diptera: Culicidae) in Central

Najmeh Hesami1; *Mohammad Reza Abai1; Hassan Vatandoost1,2; Mostafa Alizadeh3; Mahboubeh Fatemi1; Javad Ramazanpour3; *Ahmad Ali Hanafi-Bojd1,2

1Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 2Department of Environmental Chemical Pollutants and Pesticides, Institute for Environmental Research, Tehran University of Medical Sciences, Tehran, Iran 3Department of Communicable Diseases Control, Deputy for Health, University of Medical Sci- ences, Isfahan, Iran

(Received 30 May 2018; accepted 24 Apr 2019)

Abstract Background: Mosquitoes are very important vectors of diseases to human. We aimed to establish the first spatial database on the mosquitoes of , central Iran, and to predict the geographical distribution of species with medical importance. Methods: Mosquito larvae were collected from eight counties of Isfahan Province during 2014. Collected data were transferred to a database in ArcGIS and the distribution maps were created. MaxEnt model and jackknife analysis were used to predict the geographical distribution of two medical important species, and to find the effective varia- bles for each species. Results: Totally, 1143 larvae were collected including 6 species, Anopheles maculipennis s.l., An. superpictus s.l., An. marteri, Culex hortensis, Cx. theileri and Culiseta longiareolata. The area under curve in MaxEnt model was 0.951 and 0.873 rather 1 for An. maculipennis s.l. and Cx. theileri, respectively. Culex theileri had wider and more appropriate niches across the province, except for the eastern area. The environmental variable with highest gain was mean temperature of the wettest quarter for Cx. theileri and temperature seasonality for An. maculipennis. Culex theileri, An. maculipennis s.l. and An. superpictus, three important vectors of parasitic agents to humans, were collected in this study. Conclusion: The mosquito collected and mapped can be considered for transmission of malaria and filariasis in the region. Bearing in mind the results of niche modeling for vector species, more studies on vectorial capacity and re- sistance status to different insecticides of these species are recommended.

Keywords: Culicidae; Spatial distribution; Culex theileri; Anopheles maculipennis s.l.; Ecological niche modeling

Introduction

Mosquitoes are one of the most important Phlebovirus) on the inland plateau of southern groups of medical arthropods and transmit ma- Africa (3). Dirofilariasis due to Dirofilaria im- laria, filariasis, different arboviruses and en- mitis and D. repens and setariasis have been cephalitis as well as annoyance due to their reported in current studies from some parts bites (1). A serological study in 1970s showed of Iran, while West Nile Virus is also detect- West Nile infection was relatively common ed in current studies from the birds, horse, hu- in Iran with a prevalence of 30%, while in- man and mosquitoes (4–14). This is in accord- fection with Sindbis virus was very rare (2). ance with the global trends of these diseases, Culex theileri is the principal epidemic vec- although both animal and human cases of tor of Rift Valley fever virus (Bunyaviridae: this disease are under estimated (15, 16). 165 * Corresponding authors: Dr Ahmad Ali Hanafi-Bojd, http://jad.tums.ac.ir Email: [email protected], Mr Mohammad Reza Published Online: June 24, 2019 Abai, Email: [email protected]

J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche …

Study on the mosquitoes of Iran has a long and Iran as well, accurate study on the ecol- history and is conducted on different aspects ogy and bionomics of mosquitoes are neces- such as fauna, distribution, parasitic infection, sary due to their important role in disease trans- resistance to insecticides and modeling distri- mission, especially arboviruses. Data collec- bution (5, 6, 17–20). Culex theileri is reported tion on their biodiversity, distribution and ecol- from 27 out of 31 including ogy will provide guideline for appropriate vec- Ardabil, West Azarbaijan, East Azarbaijan, tor control. Bushehr, Charmahal and Bakhtiari, Fars, Gui- Geographic Information Systems (GIS) is lan, Hamadan, Hormozgan, Ilam, Isfahan, Ker- a rapidly growing technology that combines man, Kermanshah, South Khorassan, North graphics features with the environmental data Khorassan, Khorassan-e Razavi, Khuzestan, obtained from the vectors of disease. This Kohgiluyeh and Boyerahmad, Kordestan, ability helps us to assess the distribution and Lorestan, Markazi, Mazandaran, Qom, Sistan bioecology of vector species. In last two dec- and Baluchestan, Tehran, Yazd, and Zanjan ades using GIS in vector-borne diseases has (21). increased and a new field of investigation has Anopheles maculipennis s.l. is one of the been opened. Creating databases, mapping, main malaria vectors in its distribution areas spatial and statistical analysis of vector-borne including Iran (22). It is reported from 20 diseases are results of this new branch of sci- provinces of Iran including Ardabil, West ence (25). Azarbaijan, East Azarbaijan, Charmahal and This study aimed to establish the first Bakhtiari, Guilan, Golestan, Hamadan, Isfa- spatial database on the mosquitoes of Isfa- han, Kermanshah, Khorassan-e Razavi, North han Province and to predict the geographical Khorassan, Kohgiluyeh and Boyerahmad, Kor- distribution of medically important species. destan, Qazvin, Lorestan, Markazi, Mazanda- ran, Semnan, Tehran, and Zanjan (22). Materials and Methods Despite activities regarding mosquito con- trol in Iran, there is still the problem of pain- Study Area ful bites of these insects, especially in cen- The Isfahan Province covers an area of tral areas like Isfahan, Arak, Semnan, and approximately 107,027km2 and is situated in Tehran provinces. Due to the vital role of the center of Iran (Fig. 1). The province ex- health in development programs, and be- periences a moderate and dry climate, on the cause the study on ecology and bionomics of whole, ranging between 40.6 °C and 10.6 °C mosquitoes is one of the important indices on a cold day in the winter season. The av- that have a fundamental role in development erage annual temperature has been recorded of ecotourism industry, proper knowledge as 16.7 °C and the annual rainfall on an av- from behavioral characteristics and bionom- erage has been reported as 116.9mm. More ics of mosquitoes in different ecological con- than 5 million peoples are living in 24 coun- ditions is one of the main factors in planning ties of this province. Isfahan is destination of the strategy to combat the mosquitoes. Isfa- millions of tourists from different parts of han Province is one of the main poles for Iran and other countries. industry and tourism in Iran. Although rare studies have been done in past (23, 24), but Entomological Survey still there is no comprehensive survey on vec- Sampling was conducted two times dur- tor(s) bioecology in different climates, seasons, ing summer 2015 from 8 counties (Khomein- temperatures, and so on. With due attention ishahr, , Faridan, Khansar, Mo- to the extensive climate change in the world barakeh, Fereidoonshahr, , Samirom) 166 http://jad.tums.ac.ir Published Online: June 24, 2019 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … in three main topographic areas of Isfahan Bio16 (Precipitation of wettest quarter (mm)), Province. Mosquito larvae were collected by Bio17 (Precipitation of driest quarter (mm)), the standard dipping method. Coordinates of Bio18 (Precipitation of warmest quarter (mm)) the collections sites were recorded using a and Bio19 (Precipitation of coldest quarter GPS device. Species were transferred to the (mm)). Two environmental variables were al- laboratory, mounted and identified morpho- so used for modeling i.e. altitude (m) and Nor- logically (26). malized Difference Vegetation Index (NDVI). All the mounted slides were deposited in The first variable was derived from the Digi- the Medical Entomology Museum, School tal Elevation Model (DEM) of Iran with the of Public Health, Tehran University of Med- same resolution, while NDVI was acquired ical Sciences under code of GC22ST11-94. from Aug 2014 image of MODIS satellite.

Creating Database and Mapping Results All collected data obtained from this en- tomological survey were transferred to a rel- Species Composition evant database in ArcGIS and then the dis- Overall, 1143 mosquito larvae were col- tribution maps were created. lected including 6 species: Anopheles macu-

Modeling lipennis s.l. (24), An. superpictus s.l. (4), An. MaxEnt model and bioclimatic variables marteri (10), Culex hortensis (454), Cx. theileri were used to predict and to map the geo- (429) and Culiseta longiareolata (222). The graphical distribution of medically important most and the least density was due to Cx. species which had enough occurrence data hortensis (39.72%) and An. superpictus s.l points (27). Jackknife test in MaxEnt model (0.35%), respectively (Table 1). Anopheles was used to find the effective variables for maculipennis s.l. was collected from both each species. The bioclimatic data were plain and foothill areas, but we could not downloaded from the worldclim database in find this malaria vectors in mountainous ar- 1km2 spatial resolution (version1.4, eas of Isfahan Province. Culex theileri and http://www.worldclim.org/past). They were in- Cx. hortensis were the most aboundant spe- cluded Bio1 (Annual mean temperature (oC), cies. Regardless of the topography of the area, Bio 2 (Mean diurnal range: mean of monthly they were caught in all the studied areas. (max temp–min temp) (°C)), Bio3 (Isother- mality: (Bio2/Bio7)× 100), Bio4 (Tempera- MaxEnt Modeling ture seasonality (SD× 100)), Bio5 (Maximum This method was used to find the appro- temperature of warmest month (°C)), Bio6 priate niches for Cx. theileri and An. maculi- (Minimum temperature of coldest month (°C)), pennis s.l. To do this, all collection points in Bio7 (Temperature annual range (Bio5−Bio6) this study, as well as earlier studies in Isfa- (°C)), Bio8 (Mean temperature of wettest quar- han Province (1984–2015), were used to have ter (°C)), Bio9 (Mean temperature of driest enough occurrence data for modeling (Fig. quarter (°C)), Bio10 (Mean temperature of 1). Figure 2 shows the collection sites for the warmest quarter (°C)), Bio11 (Mean temper- studied species. The area under curve was cal- ature of coldest quarter (°C)), Bio12 (Annu- culated as 0.951 rather 1 for An. maculipennis al precipitation (mm)), Bio13 (Precipitation (Fig. 3). More appropriate niches for An. mac- of wettest month (mm)), Bio14 (Precipita- ulipennis were restricted to the western and tion of driest month (mm)), Bio15 (Precipi- southwestern areas (Fig. 4). Based on jack- tation seasonality (coefficient of variation)), knife test, the environmental variable with the highest gain when used in isolation is tem- 167 http://jad.tums.ac.ir Published Online: June 24, 2019 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche …

perature seasonality (Bio4), which therefore when compared against the training gain plot. appears to have the most useful information Mean temperature of wettest quarter is help- by itself. The environmental variable that ing the model to obtain a good fit to the decreases the gain the most when it is omit- training data, but the temperature seasonality ted is NDVI, which therefore appears to variable gives better results on the set-aside have the most information that is not present test data. in the other variables. These numbers show Figure 6 shows result of the jackknife test an acceptable validity for the exported maps. of variable importance for An. maculipennis For Cx. theileri, the area under curve was s.l.. The environmental variable with highest calculated as 0.873 rather 1 (Fig. 3). Based on gain, when used in isolation, was tempera- the maps, Cx. theileri had wider and more ture seasonality (Bio4). This variable appears appropriate niches across the province com- to have the most useful information for mod- paring An. Maculipennis s.l., except for the eling this species. Comparing the three jack- eastern area (Fig. 4). Figure 5 shows the result knife plots can be very informative. The AUC of the jackknife test of variable importance plot shows that isothermality (Bio3) is the most for Cx. theileri. The environmental variable effective single variable for predicting the dis- with highest gain, when used in isolation, was tribution of the occurrence data that was set mean temperature of the wettest quarter (Bio8). aside for testing when predictive performance This variable appears to have the most use- is measured using AUC, even though it was ful information for modeling this species. In hardly used by the model built using all var- Fig. 5 three jackknife plots for Cx. theileri were iables. The relative importance of isothermal- compared. The AUC plot shows that tem- ity also increases in the test gain plot, when perature seasonality (Bio4) is the most effec- compared against the training gain plot. Tem- tive single variable for predicting the distri- perature seasonality is helping the model to bution of this mosquito species used for test- obtain a good fit to the training data, but the ing. The relative importance of temperature isothermality variable gives better results on seasonality also increases in the test gain plot, the set-aside test data.

Table 1. Spatial distribution of collected mosquito larvae according to topography and species, Isfahan Province, 2015

No. and frequency of species

An. maculipennis s.l An.

An

Cs. longiareolataCs.

Cx. hortensis Cx. superpictus s.l. .

An. marteri An. County theileri Cx. Total Topography Larvae (No.)

No. % No. % No. % No. % No. % No. % Khomeinishahr Plain 129 16 12.4 2 1.56 2 1.56 12 9.3 86 66.66 11 8.52 Golpayegan Plain 50 4 8.3 2 4.2 0 0 6 12.5 36 75 0 0 Plain 65 0 0 0 0 0 0 33 50.77 32 49.23 0 0 Najafabad Plain 90 0 0 0 0 0 0 57 61.95 35 38.05 0 0 Faridan Foothill 115 4 3.47 0 0 8 6.96 0 0 34 29.57 69 60 Khansar Foothill 247 0 0 0 0 0 0 152 61.54 42 17 53 21.46 Fereidoonshahr Mountain 354 0 0 0 0 0 0 129 36.64 134 38.08 89 25.28 Samirom Mountain 93 0 0 0 0 0 0 65 69.89 28 303.11 0 0 Total 1143 24 2.1 4 0.35 10 0.88 454 39.72 429 37.53 222 19.42

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Fig.1. Study sites in Isfahan Province, Iran

Fig. 2. Spatial distribution of collection sites for Anopheles maculipennis and Culex theileri in Isfahan Province, Central Iran, 1984–2015

169 http://jad.tums.ac.ir Published Online: June 24, 2019 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche …

Fig. 3. The area under ROC curve (AUC) for Anopheles maculipennis s.l. and Culex theileri in Isfahan Province, Central Iran, 2015

Fig. 4. Probability of presence for Anopheles maculipennis s.l. and Culex theileri in Isfahan Province, Central Iran, 2015

170 http://jad.tums.ac.ir Published Online: June 24, 2019 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche …

Fig. 5. Jackknife test of AUC for Culex theileri in Isfahan Province, Central Iran, 2015

171 http://jad.tums.ac.ir Published Online: June 24, 2019 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche …

Fig. 6. Jackknife test of AUC for Anopheles maculipennis s.l. in Isfahan Province, Central Iran, 2015

Discussion In this study six Culicidae mosquito spe- cies were collected and identified. Based on the previous studies in the province, 24 mos-

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the province (23, 24). Anopheles superpictus quito species are reported as follows: Ae. was collected from Khomeinishahr and Gol- vexans, An. algeriensis, An. claviger, An. dthali, payegan Counties in our survey, but there An. maculipennis s.l., An. marteri, An. mes- are reports of this species from 12 counties seae, An. multicolor, An. sacharovi, An. su- of the province (23, 24). There is potential perpictus, An. turkhudi, Cx. modestus, Cx. for malaria transmission in the study area. hortensis, Cx. mimeticus, Cx. perexiguus, Cx. Since the province has attractions and job op- pipiens, Cx. theileri, Cx. territans, Culiseta portunities, there are likely infected foreign longiareolata, Cs. annulata, Cs. subochrea, immigrants from the endemic countries visit Ochlerotatus caspius, Oc. pulcritarsus and the area, at least in some months of the year. Uranotaenia unguiculata (16, 22, 23). Our find- Three other species in this survey were An. ings report no new record for the province. marteri, Cx. hortensis and Cs. longiareolata. The dominant species in our study was These species have no tendency to feed from Cx. hortensis (39.72%) followed by Cx. theil- human. Just Cx. hortenis known as birds ma- eri. Earlier studies in Mobarakeh County found laria vector under laboratory condition (31). Cx. theileri as the dominant species in both Culiseta longiareolatsa may rarely attack hu- larval and adult collections (23). Studies dur- man and domestic animals, although there is ing 2003–2005 were also introduced Cx. theil- little information on this species. eri as the dominant species in Isfahan Prov- MaxEnt model was used to predict the dis- ince (24). Although in our study, the current tribution of some Anopheles mosquitoes around species had the second density, it can be due the world, such as An. albimanus in Americas to the number of collection times. On the other (32), malaria vectors of Africa, Europe and hand, if field sampling is done at a better Middle East (33), and An. minimus in south- time, a greater abundance may be due to this east of Asia (34). A more recent study in Iran species. Generally Cx. theileri is a rice field used this model to find the best ecological mosquito species (28). It has usually exophi- niches for three main malaria vectors in south lic and exophagic behavior and has a high an- of Iran, i.e. An. stephensi, An. culicifacies thropophilic index, and comprised more than s.l. and An. fluviatilis s.l. (19). It is also used 77% of the mosquitoes catched on human to predict the potential areas for Cx. pipiens, bait (21). Other studies were also reported Cx. tarsalis and Ae. vexans in the United Cx. theileri as the main species in some parts States and Cx. tritaeniorhynchus in Saudi Ara- of Iran (29, 30). bia (35, 36). AUC value in this research was Culex theileri, An. maculipennis and An. 0.951 and 0.873 for An. maculipennis and superpictus as three important vectors of par- Cx. theileri, respectively. Previous studies on asitic agents to humans were collected in this MaxEnt model considered predicting AUC> study. In northwest of Iran, Cx. theileri in- 0.75 as good value for suitable niche for spe- fected was reported to D. immitis (7). There- cies (37). This suggests the MaxEnt predic- fore, in addition to numerous bites on human tion in our study is well. A new survey in in Isfahan area, it can be considered as prob- Iran reported AUC values of 0.943, 0.974 able vector of dirofilariasis. Among the col- and 0.956 for An. stephensi, An. culicifacies lected mosquitoes, two main malaria vectors s.l. and An. fluviatilis s.l., respectively (19). of Iran were identified: An. maculipennis and In other countries AUC values were reported An. superpictus. In this study, An. maculipennis between 0.77 and 0.99 for different Anophe- was only found in Khomeinishahr, Golpaye- les species (36, 38-40). This difference is due gan and Faridan Counties. However, this to various ecological needs of these species. species has reported from most counties of 173 http://jad.tums.ac.ir Published Online: June 24, 2019 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche …

Conclusion 3. McIntosh BM, Russell D, dos Santos I, Gear JH (1980) Rift Valley fever in hu- In addition to the problems caused by bites mans in South Africa. S Afr Med J. 58 on humans, they can be considered for trans- (20): 803–806. mission of malaria and filariasis in the region. 4. Siavashi MR, Massoud J (1995) Human With due attention to tourist and business at- cutaneous dirofilariasis in Iran: a report tractions of Isfahan Province, some people of two cases. Iranian J Med Sci. 20(12): from different parts of the world will travel 85–86. to different counties of the province annual- 5. Maraghi S, Rahdar M, Akbari H, Rad- ly. Considering the results of niche modeling manesh M, Saberi AA (2006) Human for vector species, it is recommended to do dirofilariasis in Ahwaz, Iran, A report additional studies on vectorial capacity of these of three cases. Pak J Med Sci. 22(2): species, their physiological age, and parasitic 211–213. infection, and insecticide resistance suscep- 6. Azari-Hamidian S, Yaghoobi-Ershadi MR, tibility status to different insecticides to pre- Javadian E, Mobedi I, Abai MR (2007) dict the risk of establishing the foci of filari- Review of dirofilariasis in Iran. J Gui- asis, West Nile fever and malaria in Isfahan lan Univ Med Sci. 15(60): 102–114. Province. 7. Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Abai MR, Mobedi I, Lin- Acknowledgements ton YM, Harbach RE (2009) Distribu- tion and ecology of mosquitoes in a

focus of dirofilariasis in northwestern Collaboration of Deputy for Health, Is- Iran, with the first finding of filarial fahan University of Medical Sciences in provid- larvae in naturally infected local mos- ing facilities for this study is highly appreci- quitoes. Med Vet Entomol. 23: 111–121. ated. Moreover, the authors are grateful to 8. Ashrafi K, Golchai J, Geranmayeh S Mr H Davoodi, technician of Museum of Med- (2010) Human subcutaneous dirofilari- ical Entomology (TUME), School of Public asis due to Dirofilaria (Nochtiella) re- Health, Tehran University of Medical Scienc- pens: clinically suspected as cutaneous es for his kind assistance for organizing of fascioliasis. Iran J Public Health. 39(1): mounted specimens. This project is financial- 105–109. ly supported by Deputy for Research, Teh- 9. Talebian A (2010) A study of West Nile ran University of Medical Sciences, Project virus infection in Iranian blood donors. No. 26818. Arch Iran Med. 13: 1–4. The authors declare that there is no con- 10. Fereidouni SR, Ziegler U, Linke S, Nie- flict of interests. drig M, Modirrousta H, Hoffmann B, Groschup MH (2011) West Nile virus References monitoring in migrating and resident water birds in Iran: are common coots 1. Service MW (1993) Mosquitoes (Culicidae). the main reservoirs of the virus in wet- In: Lane RP and Crosskey RW (ed) Med- lands? Vector Borne Zoonotic Dis. 11 ical insects and Arachnids. Chapman and (10): 1377–1381. Hall, London, pp. 120–240. 11. Chinikar S, Javadi A, Ataei B, Shakeri 2. Naficy K, Saidi S (1970) Serological sur- H, Moradi M, Mostafavi E, Ghiasi SM vey on viral antibodies in Iran. Trop Ge- (2012) Detection of West Nile virus ge- ogr Med. 22(2): 183–188. nome and specific antibodies in Iranian

174 http://jad.tums.ac.ir Published Online: June 24, 2019 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche …

encephalitis patients. Epidemiol Infect. Acta Trop. 169: 93–99. 140 (8): 1525–1529. 20. Vatandoost H, Hanafi-Bojd AA, Raeisi 12. Mardani M, Abbasi F, Aghahasani M, A, Abai MR, Nikpour F (2017) Ecolo- Ghavam B (2013) First Iranian imported gy, monitoring and mapping of insecti- case of Dengue. Int J Prev Med. 4 (9): cide resistance of malaria vector, Anoph- 1075–1077. eles culicifacies (Diptera: Culicidae) to 13. Bagheri M, Dabiri F, Terenius O, Vatan different imagicides in Iran. Asian Pac doost H, Oshaghi MA, Motazakker M, J Trop Dis. 7(1): 53–56. Asgari S, Dabiri F, Vatandoost H, Mo- 21. Hanafi-Bojd AA, Sedaghat MM (2017) hammadi Bavani M, Chavshin AR Establishment of a databank for Irani- (2015) West nile virus in mosquitoes of an mosquitoes (Diptera: Culicidae) and Iranian wetlands. Vector Borne Zoono- modeling their spatial distribution. Pro- tic Dis. 15(12): 750–754. ject No. 29953, Research Deputy, Teh- 14. Z, Chinikar S, Shakeri M, Ma- ran University of Medical Sciences. navifar L, Moradi M, Mirshahabi H, 22. Hanafi-Bojd AA, Sedaghat MM, Vatan- Jalali T, Khakifirouz S, Shahhosseini N doost H, Azari-Hamidian S, Pakdad K (2015) Prevalence of West Nile virus in (2018) Predicting environmentally suit- Mashhad, Iran: A population-based study. able areas for Anopheles superpictus Asian Pac J Trop Med. 8(3): 203–205. Grassi (s.l.), Anopheles maculipennis 15. Pampiglione S, Rivasi F (2001) Dirofilari- Meigen (sl.) and Anopheles sacharovi asis due to Dirofilaria (Nochtiella) re- Favre (Diptera: Culicidae) in Iran. Par- pens: an update of world literature from asit Vector. 11(1): 382. 1995 to 2000. Parassitologia. 42(3–4): 23. Moosa-Kazemi H, Zaim M, Zahraei-Ram- 231–254. azani AR (2000) Fauna and ecology of 16. Simon F, Lopez-Belmonte J, Macros- Culicidae in Lenjanat area, Isfahan Prov- Atxutegi C, Morchon R, Martin-Pacho ince of Iran. Armaghan Danesh J. 5 JR (2005) What is happening outside (17–18): 46–54. North America regarding human diro- 24. Ladonni H, Azari-Hamidian S, Alizadeh filariasis? Vet Parasitol. 133: 181–189. M, Abai MR, Bakhshi H (2015) The fau- 17. Zaim M, Manouchehri AV, Yaghoobi-Er- na, habitats, and affinity indices of mos- shadi MR (1985) Mosquito fauna of Iran quito larvae (Diptera: Culicidae) in Cen- (Diptera: Culicidae) 2- Culex. Iran J Pub- tral Iran. North-Western J Zool. 11(1): lic Health. 14(1–4): 1–12. 76–85. 18. Hanafi-Bojd AA, Azari-Hamidian S, Vatan- 25. Khormi HM, Kumar L (2015) Modelling doost H, Charrahy Z (2011) Spatio-tem- Interactions between Vector-Borne Dis- poral distribution of malaria vectors (Dip- eases and Environment using GIS. CRC tera: Culicidae) across different climat- Press. ic zones of Iran. Asian Pac J Trop Med. 26. Azari-Hamidian S, Harbach RE (2009) 4: 498–504. Keys to the adult females and fourth-in- 19. Pakdad K, Hanafi-Bojd AA, Vatandoost H, star larvae of the mosquitoes of Iran (Dip- Sedaghat MM, Raeisi A, Salahi-Moghad- tera: Culicidae). Zootaxa. 2078: 1–33. dam A, Foroushani AR (2017) Predict- 27. Phillips SJ, Anderson RP, Schapire RE ing the potential distribution of main ma- (2006) Maximum entropy modeling of laria vectors Anopheles stephensi, An. species geographic distributions. Ecol culicifacies s.l. and An. fluviatilis s.l. in Model. 190: 231–259. Iran based on maximum entropy model. 28. Lacey LA, Lacey CM (1990) The medical

175 http://jad.tums.ac.ir Published Online: June 24, 2019 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche …

importance of riceland mosquitoes and modeling of potential West Nile virus their control using alternatives to chem- vector mosquito species in Iowa. J In- ical insecticides. J Am Mosq Control As- sect Sci. 10: 110. soc. Suppl. 2: 1–93. 36. Al Ahmed AM, Naeem M, Kheir SM, 29. Ghavami MB, Ladonni H (2005) Fauna Sallam MF (2015) Ecological distribu- and distribution of mosquitoes (Diptera: tion modeling of two malaria mosquito Culicidae) in Zanjan Province, 2002– vectors using geographical information 2003. J Zanjan Univ Med Sci. 53: 46–54. system in Al-Baha Province, Kingdom 30. Abai MR, Azari-Hamidian S, Ladonni of Saudi Arabia. Pak J Zool. 47(6): H, Hakimi M, Mashhadi-Esmail K, 1797–1806. Sheikhzadeh K, Kousha A, Vatandoost 37. Phillips SJ, Dudík M (2008) Modeling of H (2007) Fauna and checklist of mos- species distributions with Maxent: new quitoes (Diptera: Culicidae) of East Azer- extensions and a comprehensive evalu- baijan Province, Northwestern Iran. Iran ation. Ecography. 31: 161–175. J Arthropod-Borne Dis. 1(2): 27–33. 38. Ma A, Wang JF, Wang DQ, Ren ZP (2014) 31. Santiago-Alarcon D, Palinauskas V, Prediction of potential distribution of Schaefer HM (2012) Diptera vectors of Anopheles sinensis in China based on avian Haemosporidian parasites: untan- MaxEnt. Chinese J Vec Biol Control. 25 gling parasite life cycles and their tax- (5): 393–398. onomy. Biol Rev Camb Philos Soc. 87: 39. Fuller DO, Alimi T, Herrera S, Beier JC, 928–964. Qui nones ML (2016) Spatial association 32. Fuller DO, Ahumada ML, Quiñones ML, between malaria vector species richness Herrera S, Beier JC (2012) Near-pre- and malaria in Colombia. Acta Trop. 158: sent and future distribution of Anophe- 197–200. les albimanus in Mesoamerica and the 40. Ren Z, Wang D, Ma A, Hwang J, Bennett Caribbean Basin modeled with climate A, Sturrock HJW, Fan J, Zhang W, Yang and topographic data. Int J Health Ge- D, Feng X, Xia Z, Zhou XN, Wang J ogr. 11: 13. (2016) Predicting malaria vector distri- 33. Sinka ME, Bangs MJ, Manguin S, Coet- bution under climate changes scenarios zee V, Mbogo CM, Hemingway J, Patil China: challenges for malaria elimina- AP, Temperley WH, Gething PW, Ka- tion. Sci Rep. 6: 20604. baria CW, Okara RM, Van Boeckel T, Godfray HC, Harbach RE, Hay SI (2010) The dominant Anopheles vectors of hu- man malariain Africa, Europe and the Middle East: occurrence data, distribu- tion maps and bionomic préci. Parasit Vectors. 3: 117. 34. Foley DH, Rueda LM, Peterson AT, Wilkerson RC (2008) Potential distri- bution of two species in the medically important Anopheles minimus Complex (Diptera: Culicidae). J Med Entomol. 45 (5): 852–860. 35. Larson SR, Degroot JP, Bartholomay LC, Sugumaran R (2010) Ecological niche

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