J Arthropod-Borne Dis, Dec 2022, 16(4): 278–287 N Yahaghi et al.: A Comparative Study on … 278 http://jad.tums.ac.ir Published Online: Dec 31, 2022 Original Article A Comparative Study on the Biodiversity and Species Richness of Phlebotomine Sand Flies (Diptera: Psychodidae) in Kermanshah and Khuzestan Provinces of Iran Negin Yahaghi1, Mahboubeh Fatemi1, Ahmad Ali Hanafi-Bojd1, Abdollah Naghian2, Mohammad Reza Yaghoobi-Ershadi1, Alireza Zahraei-Ramezani1, Yavar Rassi1, Hassan Soleimani3, Hossein Dehghan4, Arshad Veysi5, *Kamran Akbarzadeh1, *Amir Ahmad Akhavan1 1Department of Vector Biology and Control of Diseases, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 2Department of Medical Entomology and Vector Control, School of Health, Urmia University of Medical Sciences, Urmia, Iran 3Yazd Health Research Station, Tehran University of Medical Sciences, Yazd, Iran 4Department of Public Health, School of Public Health, Jiroft University of Medical Sciences, Jiroft, Iran 5Zoonoses Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran *Corresponding authors: Prof Amir Ahmad Akhavan; aaakhavan@tums.ac.ir, Prof Kamran Akbarzadeh; akbarzadehk@yahoo.com (Received 23 Oct 2021; accepted 07 Dec 2021) Abstract Background: Leishmaniasis is one of the most important vector-borne and neglected tropical diseases in many parts of the world. The main objective of this study was to determine the biodiversity of phlebotomine sand flies (Diptera: Psy- chodidae, Phlebotominae) in Khuzestan and Kermanshah Provinces of Iran. Methods: Sampling was conducted in Khuzestan and Kermanshah Provinces using sticky paper traps and CDC light traps. The samples were then stored in 96% alcohol-containing vials, mounted, and identified. Afterward, the alpha di- versity (using Simpson’s, Shannon-Weiner’s diversity, evenness, Maghalef’s, Menhinick’s, Hill and indices) and beta diversity indices (using Sorensen’s and Jaccard’s coefficients) were calculated. Results: A total of 4302 sand flies were caught and identified which comprised mostly of Phlebotomus papatasi, Ph. alexandri and Ph. sergenti. It was found that among the four counties of Ahvaz, Shush, Shushtar and Dezful in Khuzestan Province, Shush had the lowest, and Shushtar, the highest amount of species diversity and evenness. In the four studied counties of Kermanshah Province, species diversity in Kermanshah County had the lowest amount and Sarpol-e-Zahab, the highest. The species richness in Kermanshah County was the lowest, while Qasr-e-Shirin County had the highest amount. Conclusion: An overview of the biodiversity of phlebotomine sand flies in Kermanshah County in Kermanshah Prov- ince, and Shush County in Khuzestan Province, showed less stability in community structure of these vectors, which can be counted as an alarm for emerging dominant vectors among the studied counties and have the potential to increase the prevalence of leishmaniasis. Keywords: Leishmaniasis; Phlebotominae; Species Richness; Biodiversity; Iran Introduction Leishmaniasis is a vector-borne and neglect- ed tropical disease and a tropical infection of poverty as it is associated with malnutrition, population displacement, poor housing, weak immune system, and lack of financial resources. Among all parasitic diseases, mortality from leishmaniasis is second only to malaria (1). Leishmaniasis affects 102 countries, areas, or Copyright © 2022 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/by- nc/4.0/). Non-commercial uses of the work are permitted, provided the original work is properly cited. http://jad.tums.ac.ir/ mailto:aaakhavan@tums.ac.ir https://creativecommons.org/licenses/by-nc/4.0/ https://creativecommons.org/licenses/by-nc/4.0/ J Arthropod-Borne Dis, Dec 2022, 16(4): 278–287 N Yahaghi et al.: A Comparative Study on … 279 http://jad.tums.ac.ir Published Online: Dec 31, 2022 territories worldwide (2). The disease causes considerable human morbidity and socio-eco- nomic burden to endemic societies. Two forms of the disease, visceral leishmaniasis (VL) and cutaneous leishmaniasis (CL), are endemic in Iran, and zoonotic cutaneous leishmaniasis (ZCL) is more common (about 80%) in the ru- ral areas of 19 out of 31 provinces of the country (3). Phlebotomine sand flies (Diptera: Psy- chodidae, Phlebotominae) are the well-known vectors of leishmaniasis (4). Iran's most geo- graphic and climatic conditions are suitable for the growth and proliferation of rodents and sand flies as reservoirs and vectors of this disease (5). Up until now, 53 species of sand flies have been identified in Iran, of which 34 species be- longing to the genus Phlebotomus and 19 to the genus Sergentomyia (6). Two provinces of Khuzestan and Kermanshah were chosen acc- ording to the purposes of previous research done in 2011–2012 (7). Khuzestan Province in the southwest of Iran is considered to be an im- portant endemic focus of ZCL due to the envi- ronmental impact of the warfare (8). In 2012, the annual incidence of CL was 9.5 to 21.7 per 100000 inhabitants in the province (4). This variation may be due to migration of non-im- mune people to endemic areas, people living near rodent colonies, migration of rodents and increasing synanthropic index for the reservoir, and lack of knowledge and attitude toward ZCL (9). On the other hand, Kermanshah Prov- ince was chosen to study as a non-endemic fo- cus for CL. Alpha (or within habitats) diversity is the most common form of inventory diversity, which reflects species packing within a community. Species diversity is a central theme in ecology and has two separate components named spe- cies richness (S) and evenness (E). Two indi- ces of Shannon–Wiener (Shannon index) and Simpson’s index are commonly used for spe- cies biodiversity which differ in their empha- sis on species richness (Shannon-Wiener) or abundance (Simpson’s) (10). Beta (or between habitat) diversity is the cat- egory of differentiation diversity that measures the variation in taxonomic composition between areas of alpha diversity. Some ecological stud- ies such as species richness, species evenness, degree of presence or occurrence, synanthrop- ic index and Jaccard’s and Sorensen’s similar- ity indices are important to study the compo- sition of sand fly species in different biotopes, spatial separation among the different popula- tions and the degree of attraction or avoidance of Phlebotominae sand flies to human places (11, 12). The main purpose of this study is to de- termine species richness and biodiversity of the sand flies, and the applied purpose would be de- termining the areas with high potential in leish- maniasis transmission to implement prevention and control programs. Materials and Methods Study area Khuzestan Province (29° 57’–33° 00’N, 47° 40’–50° 33’ E) is in the southwest of the coun- try and divided into 27 counties. Topographic elevations in the province vary between 0 and 3740m (13). This province consists mostly of lowlands and is generally warm, however, north- eastern parts are more elevated and have a more moderate climate. Kermanshah Province (33° 41’–35° 17’N, 45° 24’–48° 06’E) is situated in the west part of the country and contains 14 counties. Mean topographic elevation in the province is 1342 m (14). The province is mostly mountainous, and overall, the weather condition is cool and to some extent rainy during colder seasons. Sand fly collection During the activity seasons of sand flies in 2011 and 2012, sand flies were collected using 4239 sticky paper traps and 124 CDC light traps from indoors (human dwelling and stables) and outdoors (mountainous, foothill, and plain areas) in Khuzestan and Kermanshah Provinces, shown in Fig. 1 and 2 (7). In this study, samples were http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Dec 2022, 16(4): 278–287 N Yahaghi et al.: A Comparative Study on … 280 http://jad.tums.ac.ir Published Online: Dec 31, 2022 mounted using Puri’s medium. They were then identified using the sand fly identification key of the Eastern Mediterranean Region (15). Data process and analysis To determine alpha and beta diversity, four counties from each province were selected and their data were processed in Microsoft office Excel 2016 software using related indices and coefficients. The average and standard devia- tion of all the results were calculated and, their P-value was indicated by performing the Analysis of Variance (ANOVA) test in IBM SPSS Statistics 26 software. Alpha diversity indices To determine the species diversity, Shan- non–Weiner index (H´): H´= -∑( ×ln ) was used where‘ ’ can be calculated by dividing , the number of species, by N, the total number of collected individuals (16). Also, indices Hill N₁ ( ) to determine the species diver- sity exponentially, and Hill ( ) was used where e is the Euler's number and is the symbol for Hill (17). Species richness was estimated by calcu- lating Margalef’s index ( ) which can be cal- culated through this equation: ( )= (s-1)/ln N (17) and Menhinick’s index which is more reliable (18). Evenness index (E) was calculated by di- viding H´ index by natural logarithm (ln) of the number of collected species (S) (17). To determine the dominant vector’s diver- sity, Simpson’s index (D) was calculated using the formula: . The result is a num- ber between 0 and 1, and 0 indicates unlimited diversity, and on the contrary, 1 represents no diversity at all (19). Beta diversity indices Beta diversity was also estimated intra- provincially by determining the similarity be- tween different communities using Jaccard’s (Sj) and Sorensen’s Indices (Ss). Sj: a/(a+ b+ c) and Ss: 2a/(2a+ b+ c) are the equations for calculating Jaccard’s and Sorensen’s Indices, respectively. In both equations, a represents the number of species (richness) found in both bi- otopes and b is the number of species found in the first biotope and c biotope is the number of species in the second (20). Results A total of 4302 sand flies were collected from both provinces which included 17 and 12 species belonging to the genus Phlebotomus and Sergentomyia, respectively. Species com- position and relative abundance of collected sand flies from the studied areas are shown in Table 1. 39.3% of the collected sand flies were identified as male and 60.7% as female. In Khuzestan Province, Ph. papatasi and Ph. al- exandri were the most prevalent species, which respectively consisted of 57.3% and 29.5% of the total sand flies. In Kermanshah Province, Se. dentata was the most prevalent species (29%), but it is neither a proven nor a proba- ble vector, Ph. papatasi, Ph. alexandri, and Ph. sergenti were consecutively the dominant vector species, with 24.3%, 9.1% and 9.02% of the total samples, respectively. Alpha diversity results in Table 2 show that among the four studied counties in Khuzestan province, Shushtar County had the highest prob- ability of dominant vector presence, species di- versity, and species evenness, albeit not signif- icantly (P= 0.361), also Ahvaz County showed the highest amount of species richness (P= 0.759). Shush County on the other hand, had the lowest amount of all the mentioned indices. In Kermanshah Province, Kermanshah Coun- ty also showed the lowest amount of these in- dices, whereas Javanroud County significant- ly had the highest amount of dominant vector presence (P= 0.029), Sar-e-Pol Zahab County had the highest amount of species diversity (P= 0.007) (significantly), and evenness (P= 0.132), http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Dec 2022, 16(4): 278–287 N Yahaghi et al.: A Comparative Study on … 281 http://jad.tums.ac.ir Published Online: Dec 31, 2022 and Ghasr-e- Shirin County was significantly considered to be the richest county, species-wise (P= 0.05). Beta diversity results proved that among the four studied counties in Khuzestan Province, Ahvaz and Shush County had the least amount of similarity in sand fly species, and equally, Dezful with Shushtar and Ahvaz showed the most (Table 3 and 4). As shown in Table 5 and 6, in Kermanshah Province, Javanroud County had the least similarity with Kermanshah Coun- ty and the most with Ghasr-e- Shirin County. Table 1. Species composition, abundance, and relative abundance of phlebotomine sand flies in Khuzestan and Ker- manshah Provinces, Iran, 2011–2012 Species Collection sites and Percentages Khuzestan Province % Kermanshah Province % Ph. papatasi 1425 57.344 443 24.380 Ph. alexandri 735 29.577 166 9.135 Ph. jacusieli 3 0.120 3 0.165 Ph. sergenti s.l. 13 0.523 164 9.025 Ph. mongolensis 14 0.563 1 0.055 Ph. kazeruni 1 0.0402 0 0 Ph. caucasicus group 4 0.160 1 0.055 Ph. mesghali 1 0.040 1 0.055 Ph. major 0 0 72 3.962 Ph. brevis 0 0 2 0.110 Ph. perfiliewi 0 0 13 0.715 Ph. chinensis group 0 0 53 2.916 Ph. halepensis 0 0 2 0.110 Ph. tobbi 0 0 1 0.055 Ph. keshishiani 0 0 8 0.440 Ph. wenyoni 0 0 1 0.055 Ph. longiductus 0 0 1 0.055 Se. clydei 40 1.609 16 0.880 Se. tiberiadis 56 2.253 19 1.045 Se. iranica 17 0.684 1 0.055 Se. squamipleuris 7 0.281 2 0.110 Se. dentata 75 3.018 521 28.673 Se. sintoni 76 3.058 160 8.805 Se. theodori 12 0.482 63 3.467 Se. antennata 5 0.201 88 4.843 Se. palestinensis 1 0.040 1 0.055 Se. mervynae 0 0 2 0.110 Se. africana 0 0 1 0.055 Se. pawlowskyi 0 0 8 0.440 Total 2485 100.0 1817 100.0 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Dec 2022, 16(4): 278–287 N Yahaghi et al.: A Comparative Study on … 282 http://jad.tums.ac.ir Published Online: Dec 31, 2022 Table 2. The alpha diversity indices for sand fly species in the studied counties of Khuzestan and Kermanshah Prov- inces, Iran, 2011–2012 Province County Shannon- Weiner di- versity Shannon- Weiner evenness Simpson Marghalef Menhinick Hill N₁ Hill N₂ = Khuzestan Shush 0.5933 0.2966 0.6599 0.8079 0.7776 2.0136 1.6661 Shushtar 1.2820 0.5980 0.1581 1.5383 1.1180 3.9679 3.3570 Ahvaz 0.9725 0.4682 0.3775 1.5083 1.1431 2.7669 2.4675 Dezful 1.2423 0.4813 0.3739 1.3159 0.8977 3.7509 3.1337 Kermanshah Javanroud 1.5706 0.5028 0.2527 1.9201 1.0817 4.8853 3.8484 Kermanshah 0.5703 0.3111 0.6748 0.7056 0.4768 1.8051 1.5617 Sar-e-Pol Zahab 1.5768 0.5435 0.2697 1.5537 0.8979 4.9137 3.8275 Ghasr-e- Shirin 1.5021 0.5018 0.3150 1.7301 1.7499 4.8173 3.6834 Fig. 1. Study areas in Kermanshah Province, Iran, 2011–2012 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Dec 2022, 16(4): 278–287 N Yahaghi et al.: A Comparative Study on … 283 http://jad.tums.ac.ir Published Online: Dec 31, 2022 Fig. 2. Study areas in Khuzestan Province, Iran, 2011–2012 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Dec 2022, 16(4): 278–287 N Yahaghi et al.: A Comparative Study on … 284 http://jad.tums.ac.ir Published Online: Dec 31, 2022 Table 3. The Jaccard’s and Sorensen’s coefficient (beta diversity) indices for four counties of Khuzestan Province, Iran, 2011–2012 Shush -Shushtar Shush -Ahvaz Shush -Dezful Shushtar - Ahvaz Shushtar -Dezful Ahvaz -Dezful Cj 0.54545 0.41667 0.54545 0.46667 0.69231 0.69231 Cs 0.70588 0.58824 0.70588 0.63636 0.81818 0.81818 Table 4. The Jaccard's and Sorensen's coefficient (beta diversity) indices for four counties of Kermanshah Province, Iran, 2011–2012 Javanrud - Kermanshah Javanrud - Ghasr-e-Shirin Javanrud -Sar- e-Pol Zahab Kermanshah - Ghasr-e- Shirin Kermanshah - Sar-e-Pol Zahab Sar-e-Pol Zahab - Ghasr-e-Shirin Cj 0.444444 0.578947 0.526316 0.533333 0.466667 0.5625 Cs 0.615385 0.733333 0.689655 0.695652 0.636364 0.72 Discussion This study is considered as one of the first researches on biodiversity of sand flies in Ker- manshah Province, and a complementary one in Khuzestan Province, as a main focus of CL in the southwest of Iran. Our results indicated that after more than four decades (21), Ph. papatasi and Ph. alex- andri are still active in all the studied counties, with Ph. papatasi being the dominant species. Phlebotomus papatasi normally prefers to live in plain areas rather than in mountains. Lower abundance of this species in mountainous areas such as the studied counties in Kermanshah Province could be explained by its preference to semi-arid and plain areas such as the stud- ied counties in Khuzestan Province (12, 22). Phlebotomus alexandri has been reported as a probable vector of zoonotic visceral leishman- iasis (ZVL) in Iran (7, 23). This species pre- fers regions with a high percentage of relative humidity and warmer niches (22), which may be the reason behind its higher abundance in the studied areas of Khuzestan Province, ra- ther than Kermanshah Province which is less humid and warm. From all the studied area in this study, 27 species of sand flies were collected and iden- tified. This showed that species richness of sand flies in these areas was higher than some other regions in the country (12, 24, 25). Jahanifard et al. (12) found that the urban area of Shush County has the highest biodiver- sity and evenness, and the lowest species rich- ness, which shows that the lowest species num- ber in this area became more adapted to envi- ronmental conditions. The highest species rich- ness was in the semi-urban area of this county which accounts for the high species number in peripheral areas of the county. It can be con- cluded that the natural habitat is under the stress of continuous drought in Shush County. How- ever, in the present study, this county itself showed the lowest species richness and diver- sity among the four studied counties, which could lead to a rise of activities of dominant vectors and a probable increase in leishmania- sis case reports. A study based in Kuhpayeh district in Is- fahan Province (26) revealed the importance of elevation in sand fly diversity, where the spe- cies diversity in mountainous areas was high- er than in plain areas and lowlands. The same conclusions were derived from more research throughout the recent years (25, 27), yet some indicated otherwise such as the study done by Sofizadeh et al. (28). Therefore, considering the result of the present study that shows higher di- versity in plain areas rather than elevated ones, http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Dec 2022, 16(4): 278–287 N Yahaghi et al.: A Comparative Study on … 285 http://jad.tums.ac.ir Published Online: Dec 31, 2022 the degree of species diversity cannot be simply based on the factor of elevation and, we must consider different aspects. Due to the restrictions of COVID-19, we weren’t able to collect more samples from other counties as well for much more comprehensive research. We recommend the authorities take preventive measures in Shush County in Khuzestan Province and Kermanshah County in Kermanshah Province since they may contain a more suitable habitat for vectors. Fur- ther research on the biodiversity of the remain- ing counties in both provinces and other areas of the country is highly recommended. More- over, determining the reasons behind species similarity between different counties in each province needs further research on various eco- logical, geographical, anthropological variables. Conclusions Based on the results, it can be concluded that Kermanshah County in Kermanshah Prov- ince, and Shush County in Khuzestan Prov- ince are ecologically unstable and more likely to welcome vector species, which is critical in planning control programs. Acknowledgements This study was conducted as a part of a MSc thesis of Negin Yahagi, by financial sup- ports of School of Public Health (SPH), Teh- ran University of Medical Sciences (TUMS), code of 99-2-99-49686. The authors are grate- ful to all colleagues at the University of Med- ical Sciences and declare that there is no con- flict of interest. 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