J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … 165 http://jad.tums.ac.ir Published Online: June 24, 2019 Original Article Using Ecological Niche Modeling to Predict the Spatial Distribution of Anopheles maculipennis s.l. and Culex theileri (Diptera: Culicidae) in Central Iran 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, Isfahan 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 Isfahan Province, 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 groups of medical arthropods and transmit ma- laria, filariasis, different arboviruses and en- cephalitis as well as annoyance due to their bites (1). A serological study in 1970s showed West Nile infection was relatively common in Iran with a prevalence of 30%, while in- fection with Sindbis virus was very rare (2). Culex theileri is the principal epidemic vec- tor of Rift Valley fever virus (Bunyaviridae: Phlebovirus) on the inland plateau of southern Africa (3). Dirofilariasis due to Dirofilaria im- mitis and D. repens and setariasis have been reported in current studies from some parts of Iran, while West Nile Virus is also detect- ed in current studies from the birds, horse, hu- man and mosquitoes (4–14). This is in accord- ance with the global trends of these diseases, although both animal and human cases of this disease are under estimated (15, 16). *Corresponding authors: Dr Ahmad Ali Hanafi-Bojd, Email: aahanafibojd@tums.ac.ir, Mr Mohammad Reza Abai, Email: abaimr@tums.ac.ir mailto:aahanafibojd@tums.ac.ir mailto:abaimr@tums.ac.ir J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … 166 http://jad.tums.ac.ir Published Online: June 24, 2019 Study on the mosquitoes of Iran has a long history and is conducted on different aspects such as fauna, distribution, parasitic infection, resistance to insecticides and modeling distri- bution (5, 6, 17–20). Culex theileri is reported from 27 out of 31 provinces of Iran including Ardabil, West Azarbaijan, East Azarbaijan, Bushehr, Charmahal and Bakhtiari, Fars, Gui- lan, Hamadan, Hormozgan, Ilam, Isfahan, Ker- man, Kermanshah, South Khorassan, North Khorassan, Khorassan-e Razavi, Khuzestan, Kohgiluyeh and Boyerahmad, Kordestan, Lorestan, Markazi, Mazandaran, Qom, Sistan and Baluchestan, Tehran, Yazd, and Zanjan (21). Anopheles maculipennis s.l. is one of the main malaria vectors in its distribution areas including Iran (22). It is reported from 20 provinces of Iran including Ardabil, West Azarbaijan, East Azarbaijan, Charmahal and Bakhtiari, Guilan, Golestan, Hamadan, Isfa- han, Kermanshah, Khorassan-e Razavi, North Khorassan, Kohgiluyeh and Boyerahmad, Kor- destan, Qazvin, Lorestan, Markazi, Mazanda- ran, Semnan, Tehran, and Zanjan (22). Despite activities regarding mosquito con- trol in Iran, there is still the problem of pain- ful bites of these insects, especially in cen- tral areas like Isfahan, Arak, Semnan, and Tehran provinces. Due to the vital role of health in development programs, and be- cause the study on ecology and bionomics of mosquitoes is one of the important indices that have a fundamental role in development of ecotourism industry, proper knowledge from behavioral characteristics and bionom- ics of mosquitoes in different ecological con- ditions is one of the main factors in planning the strategy to combat the mosquitoes. Isfa- han Province is one of the main poles for industry and tourism in Iran. Although rare studies have been done in past (23, 24), but still there is no comprehensive survey on vec- tor(s) bioecology in different climates, seasons, temperatures, and so on. With due attention to the extensive climate change in the world and Iran as well, accurate study on the ecol- ogy and bionomics of mosquitoes are neces- sary due to their important role in disease trans- mission, especially arboviruses. Data collec- tion on their biodiversity, distribution and ecol- ogy will provide guideline for appropriate vec- tor control. Geographic Information Systems (GIS) is a rapidly growing technology that combines graphics features with the environmental data obtained from the vectors of disease. This ability helps us to assess the distribution and bioecology of vector species. In last two dec- ades using GIS in vector-borne diseases has increased and a new field of investigation has been opened. Creating databases, mapping, spatial and statistical analysis of vector-borne diseases are results of this new branch of sci- ence (25). This study aimed to establish the first spatial database on the mosquitoes of Isfa- han Province and to predict the geographical distribution of medically important species. Materials and Methods Study Area The Isfahan Province covers an area of approximately 107,027km2 and is situated in the center of Iran (Fig. 1). The province ex- periences a moderate and dry climate, on the whole, ranging between 40.6 °C and 10.6 °C on a cold day in the winter season. The av- erage annual temperature has been recorded as 16.7 °C and the annual rainfall on an av- erage has been reported as 116.9mm. More than 5 million peoples are living in 24 coun- ties of this province. Isfahan is destination of millions of tourists from different parts of Iran and other countries. Entomological Survey Sampling was conducted two times dur- ing summer 2015 from 8 counties (Khomein- ishahr, Golpayegan, Faridan, Khansar, Mo- barakeh, Fereidoonshahr, Najafabad, Samirom) J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … 167 http://jad.tums.ac.ir Published Online: June 24, 2019 in three main topographic areas of Isfahan Province. Mosquito larvae were collected by the standard dipping method. Coordinates of the collections sites were recorded using a GPS device. Species were transferred to the laboratory, mounted and identified morpho- logically (26). All the mounted slides were deposited in the Medical Entomology Museum, School of Public Health, Tehran University of Med- ical Sciences under code of GC22ST11-94. Creating Database and Mapping All collected data obtained from this en- tomological survey were transferred to a rel- evant database in ArcGIS and then the dis- tribution maps were created. Modeling MaxEnt model and bioclimatic variables were used to predict and to map the geo- graphical distribution of medically important species which had enough occurrence data points (27). Jackknife test in MaxEnt model was used to find the effective variables for each species. The bioclimatic data were downloaded from the worldclim database in 1km2 spatial resolution (version1.4, http://www.worldclim.org/past). They were in- cluded Bio1 (Annual mean temperature (oC), Bio 2 (Mean diurnal range: mean of monthly (max temp–min temp) (°C)), Bio3 (Isother- mality: (Bio2/Bio7)× 100), Bio4 (Tempera- ture seasonality (SD× 100)), Bio5 (Maximum temperature of warmest month (°C)), Bio6 (Minimum temperature of coldest month (°C)), Bio7 (Temperature annual range (Bio5−Bio6) (°C)), Bio8 (Mean temperature of wettest quar- ter (°C)), Bio9 (Mean temperature of driest quarter (°C)), Bio10 (Mean temperature of warmest quarter (°C)), Bio11 (Mean temper- ature of coldest quarter (°C)), Bio12 (Annu- al precipitation (mm)), Bio13 (Precipitation of wettest month (mm)), Bio14 (Precipita- tion of driest month (mm)), Bio15 (Precipi- tation seasonality (coefficient of variation)), Bio16 (Precipitation of wettest quarter (mm)), Bio17 (Precipitation of driest quarter (mm)), Bio18 (Precipitation of warmest quarter (mm)) and Bio19 (Precipitation of coldest quarter (mm)). Two environmental variables were al- so used for modeling i.e. altitude (m) and Nor- malized Difference Vegetation Index (NDVI). The first variable was derived from the Digi- tal Elevation Model (DEM) of Iran with the same resolution, while NDVI was acquired from Aug 2014 image of MODIS satellite. Results Species Composition Overall, 1143 mosquito larvae were col- lected including 6 species: Anopheles macu- lipennis s.l. (24), An. superpictus s.l. (4), An. marteri (10), Culex hortensis (454), Cx. theileri (429) and Culiseta longiareolata (222). The most and the least density was due to Cx. hortensis (39.72%) and An. superpictus s.l (0.35%), respectively (Table 1). Anopheles maculipennis s.l. was collected from both plain and foothill areas, but we could not find this malaria vectors in mountainous ar- eas of Isfahan Province. Culex theileri and Cx. hortensis were the most aboundant spe- cies. Regardless of the topography of the area, they were caught in all the studied areas. MaxEnt Modeling This method was used to find the appro- priate niches for Cx. theileri and An. maculi- pennis s.l. To do this, all collection points in this study, as well as earlier studies in Isfa- han Province (1984–2015), were used to have enough occurrence data for modeling (Fig. 1). Figure 2 shows the collection sites for the studied species. The area under curve was cal- culated as 0.951 rather 1 for An. maculipennis (Fig. 3). More appropriate niches for An. mac- ulipennis were restricted to the western and southwestern areas (Fig. 4). Based on jack- knife test, the environmental variable with the highest gain when used in isolation is tem- J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … 168 http://jad.tums.ac.ir Published Online: June 24, 2019 perature seasonality (Bio4), which therefore appears to have the most useful information by itself. The environmental variable that decreases the gain the most when it is omit- ted is NDVI, which therefore appears to have the most information that is not present in the other variables. These numbers show an acceptable validity for the exported maps. For Cx. theileri, the area under curve was calculated as 0.873 rather 1 (Fig. 3). Based on the maps, Cx. theileri had wider and more appropriate niches across the province com- paring An. Maculipennis s.l., except for the eastern area (Fig. 4). Figure 5 shows the result of the jackknife test of variable importance for Cx. theileri. The environmental variable with highest gain, when used in isolation, was mean temperature of the wettest quarter (Bio8). This variable appears to have the most use- ful information for modeling this species. In Fig. 5 three jackknife plots for Cx. theileri were compared. The AUC plot shows that tem- perature seasonality (Bio4) is the most effec- tive single variable for predicting the distri- bution of this mosquito species used for test- ing. The relative importance of temperature seasonality also increases in the test gain plot, when compared against the training gain plot. Mean temperature of wettest quarter is help- ing the model to obtain a good fit to the training data, but the temperature seasonality variable gives better results on the set-aside test data. Figure 6 shows result of the jackknife test of variable importance for An. maculipennis s.l.. The environmental variable with highest gain, when used in isolation, was tempera- ture seasonality (Bio4). This variable appears to have the most useful information for mod- eling this species. Comparing the three jack- knife plots can be very informative. The AUC plot shows that isothermality (Bio3) is the most effective single variable for predicting the dis- tribution of the occurrence data that was set aside for testing when predictive performance is measured using AUC, even though it was hardly used by the model built using all var- iables. The relative importance of isothermal- ity also increases in the test gain plot, when compared against the training gain plot. Tem- perature seasonality is helping the model to obtain a good fit to the training data, but the isothermality variable gives better results on the set-aside test data. Table 1. Spatial distribution of collected mosquito larvae according to topography and species, Isfahan Province, 2015 Topography Total Larvae (No.) No. and frequency of species County A n . m a c u lip e n n is s.l A n . su p e rp ic tu s s.l. A n . m a rte ri C x . h o rte n sis C x . th e ile ri C s. lo n g ia re o la ta 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 Mobarakeh 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 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … 169 http://jad.tums.ac.ir Published Online: June 24, 2019 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 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … 170 http://jad.tums.ac.ir Published Online: June 24, 2019 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 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … 171 http://jad.tums.ac.ir Published Online: June 24, 2019 Fig. 5. Jackknife test of AUC for Culex theileri in Isfahan Province, Central Iran, 2015 J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … 172 http://jad.tums.ac.ir Published Online: June 24, 2019 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- J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … 173 http://jad.tums.ac.ir Published Online: June 24, 2019 quito species are reported as follows: Ae. vexans, An. algeriensis, An. claviger, An. dthali, An. maculipennis s.l., An. marteri, An. mes- seae, An. multicolor, An. sacharovi, An. su- perpictus, An. turkhudi, Cx. modestus, Cx. hortensis, Cx. mimeticus, Cx. perexiguus, Cx. pipiens, Cx. theileri, Cx. territans, Culiseta longiareolata, Cs. annulata, Cs. subochrea, Ochlerotatus caspius, Oc. pulcritarsus and Uranotaenia unguiculata (16, 22, 23). Our find- ings report no new record for the province. The dominant species in our study was Cx. hortensis (39.72%) followed by Cx. theil- eri. Earlier studies in Mobarakeh County found Cx. theileri as the dominant species in both larval and adult collections (23). Studies dur- ing 2003–2005 were also introduced Cx. theil- eri as the dominant species in Isfahan Prov- ince (24). Although in our study, the current species had the second density, it can be due to the number of collection times. On the other hand, if field sampling is done at a better time, a greater abundance may be due to this species. Generally Cx. theileri is a rice field mosquito species (28). It has usually exophi- lic and exophagic behavior and has a high an- thropophilic index, and comprised more than 77% of the mosquitoes catched on human bait (21). Other studies were also reported Cx. theileri as the main species in some parts of Iran (29, 30). Culex theileri, An. maculipennis and An. superpictus as three important vectors of par- asitic agents to humans were collected in this study. In northwest of Iran, Cx. theileri in- fected was reported to D. immitis (7). There- fore, in addition to numerous bites on human in Isfahan area, it can be considered as prob- able vector of dirofilariasis. Among the col- lected mosquitoes, two main malaria vectors of Iran were identified: An. maculipennis and An. superpictus. In this study, An. maculipennis was only found in Khomeinishahr, Golpaye- gan and Faridan Counties. However, this species has reported from most counties of the province (23, 24). Anopheles superpictus was collected from Khomeinishahr and Gol- payegan Counties in our survey, but there are reports of this species from 12 counties of the province (23, 24). There is potential for malaria transmission in the study area. Since the province has attractions and job op- portunities, there are likely infected foreign immigrants from the endemic countries visit the area, at least in some months of the year. Three other species in this survey were An. marteri, Cx. hortensis and Cs. longiareolata. These species have no tendency to feed from human. Just Cx. hortenis known as birds ma- laria vector under laboratory condition (31). Culiseta longiareolatsa may rarely attack hu- man and domestic animals, although there is little information on this species. MaxEnt model was used to predict the dis- tribution of some Anopheles mosquitoes around the world, such as An. albimanus in Americas (32), malaria vectors of Africa, Europe and Middle East (33), and An. minimus in south- east of Asia (34). A more recent study in Iran used this model to find the best ecological niches for three main malaria vectors in south of Iran, i.e. An. stephensi, An. culicifacies s.l. and An. fluviatilis s.l. (19). It is also used to predict the potential areas for Cx. pipiens, Cx. tarsalis and Ae. vexans in the United States and Cx. tritaeniorhynchus in Saudi Ara- bia (35, 36). AUC value in this research was 0.951 and 0.873 for An. maculipennis and Cx. theileri, respectively. Previous studies on MaxEnt model considered predicting AUC> 0.75 as good value for suitable niche for spe- cies (37). This suggests the MaxEnt predic- tion in our study is well. A new survey in Iran reported AUC values of 0.943, 0.974 and 0.956 for An. stephensi, An. culicifacies s.l. and An. fluviatilis s.l., respectively (19). In other countries AUC values were reported between 0.77 and 0.99 for different Anophe- les species (36, 38-40). This difference is due to various ecological needs of these species. J Arthropod-Borne Dis, June 2019, 13(2): 165–176 N Hesami et al.: Using Ecological Niche … 174 http://jad.tums.ac.ir Published Online: June 24, 2019 Conclusion In addition to the problems caused by bites on humans, they can be considered for trans- mission of malaria and filariasis in the region. With due attention to tourist and business at- tractions of Isfahan Province, some people from different parts of the world will travel to different counties of the province annual- ly. Considering the results of niche modeling for vector species, it is recommended to do additional studies on vectorial capacity of these species, their physiological age, and parasitic infection, and insecticide resistance suscep- tibility status to different insecticides to pre- dict the risk of establishing the foci of filari- asis, West Nile fever and malaria in Isfahan Province. Acknowledgements Collaboration of Deputy for Health, Is- fahan University of Medical Sciences in provid- ing facilities for this study is highly appreci- ated. Moreover, the authors are grateful to Mr H Davoodi, technician of Museum of Med- ical Entomology (TUME), School of Public Health, Tehran University of Medical Scienc- es for his kind assistance for organizing of mounted specimens. 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