Determining the Fauna of Mosquitoes (Diptera: Culicidae) and Probable Infection to West Nile Virus in Lorestan Province, Western Iran http://jad.tums.ac.ir Published Online: Dec 31, 2021 J Arthropod-Borne Dis, Dec 2021, 15(4): 397–404 SH Moosa-Kazemi et al.: Determining... Original Article Investigation on Mosquitoes Fauna (Diptera: Culicidae) and Probable Vector of West Nile Virus in Lorestan Province, Western Iran *Seyed Hassan Moosa-Kazemi1, Yadollah Etemadi1, Mohammad Mehdi Sedaghat1, Hassan Vatandoost1,2, Hamid Mokhayeri3, *Mohammad Hassan Kayedi4 1Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 2Institute for Environmental Research, Tehran University of Medical Sciences, Tehran, Iran 3Department of Communicable Diseases Control and Prevention, Health Center, Lorestan University of Medical Sciences, Khorramabad, Iran 4Razi Herbal Medicines Research Center and Department of Parasitology and Mycology, School of Medicine, Lorestan University of Medical Sciences, Khorramabad, Iran *Corresponding author: Dr Mohammad Hassan Kayedi, E-mail: kayedi78@yahoo.co.uk, Dr Seyed Hassan Moosa-Kazemi, E-mail: moosakazemi@tums.ac.ir (Received 15 Dec 2019; accepted 30 Dec 2021) Copyright © 2021 The Authors. Published by Tehran University of Medical Sciences.Copyright © 2021 The Authors. Published by Tehran University of Medical Sciences. This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International license (https://creativecommons.org/licenses/This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International license (https://creativecommons.org/licenses/ by- nc/4.0/). Non-commercial uses of the work are permitted, provided the original work is properly cited.by- nc/4.0/). Non-commercial uses of the work are permitted, provided the original work is properly cited. Abstract Background: Fauna and larval habitat characteristics studies on mosquitoes are important tools to identify the breeding places of the vectors and management of the control strategies. This study was done to provide data on Culicidae fauna, larval habitat characteristics and identifying poten- tial vectors of West Nile virus in Lorestan Province, west of Iran. Methods: Culicidae mosquitoes were collected at three counties and nine site stations from Lo- restan Province, west of Iran in 2017. Adult mosquitoes were collected using human and animal bite collection methods, New Jersey and CDC light traps and pit shelters by aspirator. Larva were collected by dipping method. RT-PCR technique was employed for detection of the West Nile virus among mosquito’s samples. Results: 4805 mosquitoes were collected from three counties and nine sites in Lorestan Province during June–October 2017, including 4363 adults and 442 larvae. The most abundant species col- lected from all counties in both adult and larval stages were Culex pipiens (49.10%), Cx. theileri (31.82%), Anopheles maculipennis (11.09%), An. superpictus (2.66%), An. stephensi (2.12%), Cx. perexiguus (1.89%), An. dthali (1.17%) and An. sacharovi (0.15%) respectively. West Nile virus was detected in none of mosquitoes examined. Conclusion: The results of this study revealed that arbovirus vectors such as Cx. pipiens along with Cx. theileri and Cx. perexiguus are well adapted to a broad range of habitats and different climatic conditions in Lorestan Province. That necessitates further routine surveillance of arbo- viral infections. Keywords: Anopheles; Arboviruses; Culex; West Nile; Habitat Introduction Mosquitoes (Diptera: Culicidae) are the medically-important species for malaria, filariasis, encephalitis and some other arboviral diseases transmission (1-3). The Culicidae family include 2 subfamilies, 41 genera and 3584 species (4). The most 398 http://jad.tums.ac.ir Published Online: Dec 31, 2021 J Arthropod-Borne Dis, Dec 2021, 15(4): 397–404 SH Moosa-Kazemi et al.: Determining... important genera of the family are Anopheles, Culex and Aedes. Mosquitoes are vectors of important vector-borne diseases malaria, filariasis, dengue fever, yellow fever, chikungunya, west Nile Virus and Zika Virus which are among the greatest health problems in the world (5- 7). Considering the fact that in Lorestan Province, Iran, some vector mosquitoes of diseases such as West Nile, dirofilariasis and malaria are present; study on the composition, distribution and ecology of mosquitoes have great impacts in vector control programs. These findings guide us for better planning of disease control strategies. Regards to new human activities and weather change in the research area, the outcomes of our investigation should helps health services to management vectors increasing and establishment in the area, therefore, the risk of transmission of diseases by mosquitoes gets minimized. The aim of the present study has been determining of the composition, distribution and some ecological aspects of mosquitoes in Lorestan Province, Iran, which is of high medical importance from the point of view of the arboviral vectors. Materials and Methods Study areas Lorestan Province is located in western Iran, between 32º 40´-32 º 34´ N latitudes and 46º50´-46º 51´ E longitudes. The province covers an area of approximately 28,308 km² with a population of around 1,800,000 people (Fig. 1, Table 1). This province contains 11 counties with one million people called metropolitan. Out of them, Khorramabad, with a population of 800,000, is ranked amongst the 40 most populous metropolitan cities of Iran. The hottest months of the year are from mid- July to mid-September when temperatures range from 28 °C to 40 °C and the coldest month’s experience 1 °C around December– January, but at certain times in winter it can reach −15 °C. Khorramabad County has moderate winters and hot summers. Average annual rainfall is approximately 516 millimeters, the maximum rainfall has been recorded during the winter season. On the whole, the province has a semi-arid, steppe climate in the south and Mediterranean climate in the north. (Fig. 1, Table 1). Fig. 1. Map of Iran and locations of study areas in Lorestan Province, Iran Fig. 1. Map of Iran and locations of study areas in Lorestan Province, Iran https://en.wikipedia.org/wiki/Semi_arid https://en.wikipedia.org/wiki/Alpine_climate 399 http://jad.tums.ac.ir Published Online: Dec 31, 2021 J Arthropod-Borne Dis, Dec 2021, 15(4): 397–404 SH Moosa-Kazemi et al.: Determining... Mosquito collection and species Identification For mosquito collection, nine sites with different biotopes in Khorramabad, Selseleh (Alashtar) and Chegeni Counties were selected (Fig. 1, Table 1). In this study, the collection of mosquito larvae was performed in different habitats using the standard dipping technique (using 350 ml Clark’s dippers) and whirl pack bags (8). CDC and New Jersey light traps, animal and human bites and shelter pit methods were used for collecting mosquitoes. Mosquitoes capture was done during June to October 2017. Larvae and adult mosquitoes were identified by morphological keys (9). Physical and biological characteristics of larval habitats The ecological characteristics containing geographical data of collecting sites (latitude, longitude and altitude), type of habitat (stagnant, stream, seepage and water container), vegetation situation (presence or lack of vegetation), kind of vegetation (leaf- Null, Oryza sativa, Typha latifolia, Carex dipsacea and Acorus calamus), turbidity, exposure to sunlight (full, partial sunlight and covered or shaded), depth, substrate type (muddy, sandy, rocky and concrete), distance from animal and human houses and physicochemical attributes such as water temperature were recorded (7-9, 10). Statistical analyses The species richness (R: Margalef index), unified indices (D: Simpson’s diversity index and H: Shannon–Wiener index) and evenness (E: distribution of abundances among the species) as measures of diversity, were calculated for Lorestan Province and different study counties. Below is the formulae and their rationale for our research: 1 S R ln N − = ( ) ( )1 1 1 1 S i i i n n D N N= − = − −∑ ( ) ( ) 1 S i i i H p ln p =  ∆ =  ∑ ( ) H E ln s ∆ = Results In total, 4363 adults and 442 larvae were collected from three counties and nine sites in Lorestan Province during June–October 2017. The properties of geographical larval habitats (latitude, longitude and altitude) have been shown in Fig. 1 and Table 1. West Nile virus was not detected in mosquitoes. An. maculipennis s.l., An. superpictus s.l, Cx. perexiguus, Cx. pipiens, and Cx. theileri, were collected at both adult and larval stages (Table 2). Table 1. Geographical characters of the collection sites, Lorestan Province, Iran Code Locations County Geographical situation Longitude (E) Latitude (N) Altitude (M) Topography No M Robat Namaki Khorramabad 48° 18' 34.67'' E 33° 36' 22.79'' N 1302.76 m Mountain 1 P Sarzangoleh Khorramabad 48° 18' 2.10'' E 33° 26' 8.29'' N 1152.29 m Plain 2 D Dast Be Zanoo Khorramabad 48° 19' 12.68'' E 33° 26' 23.79'' N 1164.07 m Slope 3 D Cham Divan Chegeni 48° 0' 29.78'' E 33° 30' 19.69'' N 1003.74 m Slope 4 P Sharaf Bostanrood Chegeni 47° 56' 29.11'' E 33° 26' 37.42'' N 957.95 m Plain 5 M Berkeh Chegeni 48° 1' 3.39'' E 33° 33' 15.83'' N 1110.27 m Mountain 6 M Chartakteh Selseleh 48° 17' 41.56'' E 33° 47' 51.83'' N 1715.29 m Mountain 7 P Varnamad Selseleh 48° 8' 50.07'' E 33° 44' 19.74'' N 1565.05 m Plain 8 D Kakareza Selseleh 48° 15' 39.02'' E 33° 43' 17.51'' N 1572.64 m Slope 9 Table 1. Geographical characters of the collection sites, Lorestan Province, Iran 400 http://jad.tums.ac.ir Published Online: Dec 31, 2021 J Arthropod-Borne Dis, Dec 2021, 15(4): 397–404 SH Moosa-Kazemi et al.: Determining... The most abundant species collected from all counties in both adult and larval stages were Cx. pipiens, Cx. theileri, An. maculipennis s.l., An. superpictus s.l. , An. stephensi, Cx. perexiguus, An. dthali and An. sacharovi respectively. Some species such as Cx. pipiens, Cx. theileri, An. maculipennis s.l. have wide distribution in the study areas, but some species such as An. stephensi have been collected from limited areas (Table 2). In larvae and adult stages of mosquitoes, two genera along with 7 species were collected and identified from Khorramabad County. Culex pipiens, Cx. theileri, An. superpictus s.l., An. maculipennis s.l., Cx. perexiguus, An. dthali and An. sacharovi were the most abundant species respectively (Table 2). In Chegeni County, two genera including 8 species were identified: Cx. pipiens, Cx. theileri, An. maculipennis s.l., An. stephensi, An. superpictus, Cx. perexiguus, An. dthali and An. sacharovi (Table 2). In Selseleh County, five species in two genera were identified: Cx. theileri, Cx. pipiens, Cx. perexiguus, An. Maculipennis s.l. and An. dthali (Table 2). Characteristics of mosquito larval habitats Khorramabad and Chegeni larval sites had stagnant water while Selseleh had seepage water. The characteristics of Chegeni and Selseleh Counties were more similar than Khorramabad County. Both Chegeni and Selseleh Counties had larval sites with turbid water, muddy substrate, and shallow depth. In addition, these sites were covered by sunlight with leaf-Null, Oryza sativa, Typha latifolia, Carex dipsacea and Acorus calamus, vegetation. We found stagnant and clear water without vegetation with exposed to sunlight. The sites were away from human and animal houses, around more than two Table 2. Composition and abundance percentage of collected species from larval habitats and adult mosquitoes in the Lorestan Province of Iran, June–October 2017 Province Location species Larvae Adult No. % No. % Lorestan Khorramabad An. dthali 0 0 32 1.91 An. superpictus s.l. 0 0 57 3.41 An. sacharovi 0 0 2 0.11 An. maculipennis s.l. 14 5.90 27 1.61 Cx. pipiens 124 52.32 988 59.26 Cx. theileri 89 37.55 535 32.09 Cx. perexiguus 10 4.21 26 1.55 Total 237 100 1667 100 Chegeni An. dthali 0 0 23 0.88 An. superpictus s.l. 9 5.62 62 2.39 An. stephensi 0 0 102 3.94 An. sacharovi 0 0 5 0.193 An. maculipennis s.l. 24 15 466 18 Cx. pipiens 87 54.37 1090 42.11 Cx. theileri 34 21.25 795 30.71 Cx. perexiguus 6 3.75 45 1.73 Total 160 100 2588 100 Selseleh An. maculipennis s.l. 1 2.22 1 0.92 Cx. perexiguus 4 8.88 0 0 Cx. pipiens 18 40 52 48.14 Cx. theileri 22 48.88 54 50 An.dthali 0 0 1 0.92 Total 45 100 108 100 Total 442 100 4363 100 Table 2. Composition and abundance percentage of collected species from larval habitats and adult mosquitoes in the Lorestan Province of Iran, June–October 2017 401 http://jad.tums.ac.ir Published Online: Dec 31, 2021 J Arthropod-Borne Dis, Dec 2021, 15(4): 397–404 SH Moosa-Kazemi et al.: Determining... kilometers. In such a larval breeding site, the water temperature was 23 °C. In this larval habitat, one Anophelinae (An. maculipennis s.l.) and three Culicinae species of Cx. theileri, Cx. perexiguus, and Cx. pipiens were collected (Tables 2, 3). According to the results, presented in tables 2 and 3, larvae of mosquitoes were observed in all different types of the habitats. In addition, our results showed that Cx. pipiens, and Cx. theileri, had the most distribution and adaptation to different types of larval habitats, respectively. These mosquitoes larvae were captured in most sites but, Cx. perexiguus was found only in the shallow, stagnant, and turbid water, covered with plants and with a muddy substrate. In addition, the distribution of An. sacharovi was limited and only collected in the habitats with seepage, stagnant and turbid water along with muddy substrate and shallow depth at Sharaf Boostanrood of Chegeni. An. sacharovi was found only in paddy fields, having stagnant and clean water with a muddy substrate exposed to sunlight. We found differences in the species diversity, due to Simpson’s diversity index, Shannon-Wiener index (H’), and species richness of the mosquitoes in the study areas of Lorestasn Province (Table 4). The species richness and the three indices were found to be minimum in Selseleh County (R= 0.640; D= 0.318; H’= 0.782; E= 0.564), whereas the estimated diversity (D= 0.458; H’= 1.008), and richness (R= 0.809) were the highest in Khorramabad County. Discussion The present research is the first study on distribution, diversity and ecology of mosquitoes, with emphasis on Cx. pipiens as potential arbovirus vectors in Lorestan Province, western Iran. Lorestan Province contains diverse geographical areas with different climates. These diverse conditions can provide a suitable environment for the establishment of different species of mosquitoes that can justify the variety of mosquito species in this region. This study showed many mosquito species had ecological adaptations in this area. In spite of these eco-biological characteristics, the Table 3. Characteristics of mosquito larval collection sites in three counties of Lorestan Province of Iran, June– October 2017 County Type Tur Exp Veg DHH DAH Depth Sub T Khorramabad Stagnant Clear Exposed Without >2km >2km <1m Muddy 23 Chegeni Stagnant Turbid Covered leaf-Null, Oryza sativa, Typha latifolia, Carex dipsacea >2km 500m Shallow Muddy 9 Selseleh Seepage water Turbid Covered leaf-Null, Carex dipsacea and Acorus calamus, >2km 200m Shallow Muddy 13 ND: not determined, Tur: Turbidity, Exp: Sun exposure, Veg: Vegetation type, DHH: Distance from the nearest human houses, DAH: Distance from the nearest animal house, Sub: Substrate type, T: Temperature. Table 3. Characteristics of mosquito larval collection sites in three counties of Lorestan Province of Iran, June– October 2017 Table 4. The species richness (R), Simpson's diversity index (D), Shannon-Weiner diversity index (H)̕, and evenness (E) of the adult collected mosquitoes in the study areas County S R D H̕ E Khorramabad 7 0.809 0.458 1.008 0.519 Chegeni 8 0.763 0.490 1.353 0.650 Selseleh 4 0.640 0.318 0.782 0.564 Table 4. The species richness (R), Simpson’s diversity index (D), Shannon-Weiner diversity index (H)̕, and evenness (E) of the adult collected mosquitoes in the study areas 402 http://jad.tums.ac.ir Published Online: Dec 31, 2021 J Arthropod-Borne Dis, Dec 2021, 15(4): 397–404 SH Moosa-Kazemi et al.: Determining... ecology of mosquitoes present in Lorestan Province is largely unknown. In the present investigation we tried to study distribution and ecology of mosquitoes in three northeastern, northwest and central regions of Lorestan Province. Although some studies had been conducted on fauna and checklist of mosquitoes in parts of this region based on our best knowledge, no studies have been done earlier on the ecology of mosquitoes in these regions (11, 12). In the current study, two genera and eight species were collected and identified. For the first time, Cx. perexiguus species was reported from Chegeni and Selseleh Counties. Some studies had reported An. dthali, An. sacharovi, An. maculipennis s.l., and An. superpictus s.l. in Lorestan Province (13, 14). In our study, for the first time, An. stephensi and An. sacharovi were found in Chegeni, however, in previous studies the existence of these species was not reported in such areas (11-13). Some investigations reported Culiseata annulata and Cs. subochrea in Lorestan Province and Cs. subochrea in Khuzestan Province (11-13, 15). Culiseta longiareolata species was reported as the most abundant mosquito in Kermanshah, Kurdistan and Sistan and Baluchistan Provinces (16, 17). Comparing the results of our study with a recent study carried out in western Iran (10) showed that four species (An. maculipennis, An. superpictus, Cx. pipiens and Cx. theileri) were common between Lorestan and west Azerbaijan Provinces. The results of our study compared with the results of research conducted in Zanjan Province (18), showed that four species (An. maculipennis s.l., An. superpictus s.l., Cx. pipiens, and Cx. theileri, were common between these two provinces. The comparison of the results of our study with a recent study conducted in Kurdistan Province (19) showed that four species (An. maculipennis s.l., An. superpictus s.l., Cx. theileri and Cx. pipiens) are common between two provinces. In Turkey (20), and in the provinces of Ardabil, Kurdistan and West Azarbaijan of Iran, Cx. theileri and Cx. pipiens were dominant and most abundant species in the area (21) and our study is in line with such results. The climate changes and biotic and abiotic environment factors, including plants, temperature and rainfall ranges, significantly affect the type and frequency of larval mosquito habitats. The mentioned factors have impacts on the longevity, larval stages, number of mosquitoes, behavior and adult development of mosquitoes. As a result, the transmission of diseases through mosquitoes is directly affected by environmental factors (22, 23). The presence of plants as a source of sugar for mosquitoes is very important that influence both larval and adult stage development (24, 25). Plants provide energy for mosquitoes. As a result, the survival rate will increase and the longevity of mosquitoes will be longer than the extrinsic incubation period of the parasite, therefore the incidence of disease increases (26, 27). In our study, four species of plants such as Leaf-Null, Oryza sativa, Typha latifolia, Carex dipsacea and Acorus calamus were found in relation to mosquito larval habitats. Few studies have been carried out on plant species in collaboration with mosquito species in Iran. In our study, various genera of mosquitoes such as Anopheles and Culex were found in relation with various plants. Aedes vexans and Ae. caspius have been reported earlier in these areas (11-13). The results of our research show that climate changes in association with human activities effect on the species distribution in the area. Abundance of species of mosquitoes related to physio-chemical characteristics of larval sites. For example, Culex species were captured from different larval sites, determining that Culex species survived in a range of water habitats. Larval habitats in this study were stagnant, stream and seepage, water container, turbid and clear water, sun exposed or covered from sunlight, with a rocky or muddy substrate and shallow depth. Studies showed that some of Culex larval species were found alone or along with other mosquitoes, such as Anopheles and Aedes (29-31), which has been observed in 403 http://jad.tums.ac.ir Published Online: Dec 31, 2021 J Arthropod-Borne Dis, Dec 2021, 15(4): 397–404 SH Moosa-Kazemi et al.: Determining... our study. The results of some studies showed that there is a significant relationship between the distance of larval habitats of Anopheles mosquitoes and human and animal sites. These studies suggested that Anopheles mosquitoes are found more often near human and animal houses (32). Our study showed that there is a significant correlation between the distance of larval habitats of Anopheles and Cx theileri with animal and human dwellings due to larval sites of both species are more near to animal and human dwellings. This association was not found between the larval sites of Cx. pipiens and with human and animal houses because the habitats of these mosquitoes were found at various intervals from human and animal houses. Conclusion The results of this study revealed that arbovirus vectors such as Cx. pipiens along with Cx. theileri and Cx. perexiguus are well adapted to a broad range of habitats and different climatic conditions in Lorestan Province. Determining of distribution and full description of ecology of arboviral vectors under local eco-demographic conditions in Lorestan Province have provided important ecological information on establishment of important mosquito borne diseases and help with minimizing the risk of transmission of disease by mosquitoes. 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Am J Trop Med Hyg. 67(1):32-8. https://pubmed.ncbi.nlm.nih.gov/?term=Toure%2BMB&cauthor_id=20854666 https://pubmed.ncbi.nlm.nih.gov/?term=Traore%2BMM&cauthor_id=20854666 https://pubmed.ncbi.nlm.nih.gov/?term=Traore%2BMM&cauthor_id=20854666 https://pubmed.ncbi.nlm.nih.gov/?term=Bah%2BS&cauthor_id=20854666 https://pubmed.ncbi.nlm.nih.gov/?term=Doumbia%2BS&cauthor_id=20854666 https://pubmed.ncbi.nlm.nih.gov/?term=Schlein%2BY&cauthor_id=20854666 Investigation on Mosquitoes Fauna (Diptera: Culicidae) and Probable Vector of West Nile Virus in Lor Abstract Keywords Introduction Materials and Methods Study areas Mosquito collection and species Identification Physical and biological characteristics of larval habitats Statistical analyses Results Characteristics of mosquito larval habitats Discussion Conclusion Acknowledgements Competing interest References