J Arthropod-Borne Dis, June 2021, 15(2): 225–235 S H Hosseini et al.: The Effect of … 225 http://jad.tums.ac.ir Published Online: June 30, 2021 Original Article The Effect of Geographical and Climatic Factors on the Distribution of Phlebotomus papatasi (Diptera: Psychodidae) in Golestan Province, an Endemic Focus of Zoonotic Cutaneous Leishmaniasis in Iran, 2014 Seyed Hamid Hosseini1,2, Ehsan Allah-Kalteh3; *Aiuob Sofizadeh4 1School of Health, Tehran University of Medical Sciences, Tehran, Iran 2Vector borne Diseases Research Center, North Khorasan University of Medical Sciences, Bojnurd, Iran 3Health Management and Social Development Research Center, Golestan University of Medical Sciences, Gorgan, Iran 4Infectious Disease Research Center, Golestan University of Medical Sciences, Gorgan, Iran *Corresponding author: Dr Aiuob Sofizadeh, E-mail: a_sofizadeh@yahoo.com (Received 9 Feb 2018; accepted 21 Jun 2021) Abstract Background: Phlebotomus papatasi is known as the main vector of zoonotic cutaneous leishmaniasis. This study aimed to investigate the effect of geographical and bioclimatic factors on the Ph. papatasi distribution. Methods: A total of 34 villages were selected, and sampling was performed three times using 120 sticky traps in each selected village. All the collected species were mounted and identified their species. The densities of Ph. papatasi were measured in all the villages and entered into ArcMap as a point layer. The required bioclimatic and environmental vari- ables were extracted from the global climate database and The normalized difference vegetation index was obtained from the MODIS satellite imagery, also, all variables entered into ArcMap as raster layers, so The numerical value of each independent variable in the cell where the selected village is located in this, was extracted using spatial analyst tools and the value to point submenu. All the data were finally entered into IBM SPSS, and the relationship was exam- ined between the number of collected Ph. papatasi and the independent variables using Spearman's correlation test. Results: A total of 1773 specimens of Ph. papatasi were collected. The findings of this study showed that max tem- perature of warmest month, temperature annual range, temperature seasonality, mean diurnal range, precipitation sea- sonality, mean temperature of driest and warmest quarter were positively associated with the density of Ph. papatasi. Conclusion: Air temperature and precipitation were shown as the most significant factors in the distribution of Ph. pa- patasi. Keywords: Ecology; Phlebotomine sand fly; GIS Introduction Leishmaniasis is one of the most important vector-borne parasitic diseases and appears as a significant health problem in Iran. Cutaneous and visceral leishmaniasis are two types of the disease in Iran. The cutaneous leishmaniasis (CL) is also prevalent in two forms of anthro- ponotic cutaneous leishmaniasis (ACL) and zoonotic cutaneous leishmaniasis (ZCL) in the country (1). Different studies conducted in Iran showed that vectors for ACL and ZCL were Phlebotomus sergenti and Phlebotomus papa- tasi, respectively (1-3). In Golestan Province as one of the most im- portant ZCL foci in Iran (4-8), Leishmania major is the agent and wild rodents such as Rhombomys opimus and Meriones libycus are reservoir hosts of ZCL (9-11). In a wide range of similar studies conducted in the province, Ph. papatasi was shown as the main ZCL vector and the infection range of Ph. papatasi to L. major was reported as 10% (11-12). Further, various studies con- ducted in the province showed the CL incidence equal to 31.7 per 100,000 people. among them, the two counties of Gonbad-e Kavus and 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/by- nc/4.0/). Non-commercial uses of the work are permitted, provided the original work is properly cited. http://jad.tums.ac.ir/ https://creativecommons.org/licenses/by-nc/4.0/ https://creativecommons.org/licenses/by-nc/4.0/ J Arthropod-Borne Dis, June 2021, 15(2): 225–235 S H Hosseini et al.: The Effect of … 226 http://jad.tums.ac.ir Published Online: June 30, 2021 Maraveh Tappeh located in the northeast of the province had the highest incidence rates of 153 and 117 per 100,000 people (13). During 2010– 2017, 360–1766 people from all age and gender groups in the province were infected with CL annually (14). Compared to the other regions of the province, the vectors and reservoirs of the disease are more abundant in the northeastern region of the province and the disease has high- er incidence. These differences could be reasons for the geographical and climatic susceptibi- lity of the region to a higher prevalence of the disease (13, 15). Leishmaniasis is naturally dependent on en- vironmental factors and climate change (16), and the environment plays a significant role in the transmission of the disease (17). Due to different species of agents and vectors, en- vironmental changes can have various effects on the transmission of leishmaniasis in dif-ferent regions of the world (18). Hence, environmental factors and climate change may significantly affect the growth, development, and distribution of Ph. papatasi as the main ZCL vector. Tem- perature and relative humidity are known as the most significant factors associated with the distribution of Ph. papatasi (19), and the cli- mate change that has taken place in recent years has become a critical factor in the distribution of this species (17). It is also believed that the wide distribution of this species in the nature is dependent on environmental conditions and many of these conditions are measurable (20). Therefore, in recent years, many studies have been carried out on finding effective factors in the distribution of Ph. papatasi and several factors have been considered as essential factors in the distribution of this species. In a study conducted in Golestan Province (21), slope, altitude, annual mean temperature, and the normalized difference vegetation index (NDVI) were introduced as the most significant factors in the distribution of Ph. papatasi. Another study conducted in Iran (22) also reported the mean temperature of the wettest quarter, slope, pre- cipitation seasonality, and the precipitation of the wettest quarter as major factors associated with the distribution of this species. A study conducted in Eastern Mediterranean (23) re- vealed that land cover, mean temperature of coldest quarter, max temperature of warmest month, and min temperature of coldest month were the most critical factors for the distri- bution of Ph. papatasi. Further, in a study conducted in Libya (20), the altitude from the sea level was reported as a major factor asso- ciated with the distribution of Ph. papatasi. Given the significance of Ph. papatasi in the transmission of CL in Golestan Province, as well as the climate diversity of different re- gions in the province, the present study was carried out to examine the effect of different geographical and climatic factors (mentioned in the materials and methods section) on the distribution of Ph. papatasi. Materials and Methods Study area Golestan Province is one of the 31 prov- inces of Iran, located in the north-east of the country, south of the Caspian Sea (53°57′- 56°23′ E, 36°30′-38°08′ N) and makes ap- proximately 1.3% of Iran's total area with a landmass of 20437.74 square km. This pro- vince is located between the three provinces of Mazandaran, Semnan and North Khorasan, is bordered by Turkmenistan from the north. The province is connected to the Caspian Sea from the east and to Alborz Mountains from the south. Weather conditions are largely di- verse in various regions of the province. As such, one can experience mountainous climates in the south part of the province, arid and semi- arid climate in the north part, and mild Medi- terranean climate in the western and central regions. In 2019, the province had maximum and minimum air temperatures of 40 and 20 mm, respectively, maximum and minimum re- lative humidity of 70 and 90%, respectively, and a rainfall amount of 333ml. It can be concluded that a wide range of suitable cli- http://jad.tums.ac.ir/ https://en.wikipedia.org/wiki/Iran https://en.wikipedia.org/wiki/Caspian_Sea J Arthropod-Borne Dis, June 2021, 15(2): 225–235 S H Hosseini et al.: The Effect of … 227 http://jad.tums.ac.ir Published Online: June 30, 2021 matic and geographical conditions are avai- lable for the development of various insect species in the province (24). Sand fly collection This analytical cross-sectional study was carried out from July to September 2014 by performing a three-time capture in a total of 34 villages (2–4 villages in each county). Sticky paper traps coated with Castor oil were used to collect sand flies. For each village, 60 in- door and 60 outdoor sticky paper traps were installed before the sunset and collected the following morning before the sunrise. All the collected sand flies were placed in acetone for two minutes and stored in 70% ethanol before transferring to the laboratory. In the labora- tory, microscopic slides of the specimens were provided and the specimens were mounted in Puri’s medium. Species of all the sand flies were determined using relevant morpholo-gical keys (25-26). The data were analyzed using Spearman's correlation test in IBM SPSS ver- sion 22.0. Study variables In this study, we used 22 geographical and climatic variable including: Alt: altitude from sea level (m) (Alt), Slope: slope in degrees obtained from altitude (%), BIO1: annual mean temperature (°C), BIO2: mean diurnal range (monthly mean (max temp-min temp)) (°C), BI03: isothermality (BIO2/BIO7) (×100), BIO4: temperature seasonality (standard deviation × 100), BIO5: max temperature of warmest month (°C), BIO6: min temperature of coldest month (°C), BIO7: temperature annual range (BIO5- BIO6) (°C), BIO8: mean temperature of wettest quarter (°C), BIO9: mean temperature of driest quarter (°C), BIO10: mean temperature of warmest quarter (°C), BIO11: mean tempera- ture of coldest quarter (°C), BIO12: annual precipitation (mm), BIO13: precipitation of wettest month (mm), BIO14: precipitation of driest month (mm), BIO15: ), BIO16: precip- itation of wettest quarter (mm), BIO17: precip- itation of driest quarter (mm), BIO18: precipi- tation of warmest quarter (mm), BIO19: pre- cipitation of coldest quarter (mm), NDVI: normalized differentiated vegetation index. Bioclimatic variables (n=19), environmen- tal variables including altitude and slope, and NDVI were independent variables. The bio- climatic variables were obtained from the WorldClime global climate database (http://www.worldclim.org/current) at a spa- tial resolution of 1km2. These variables were derived from long-term (1950–2000) monthly rainfall and temperature values for the devel- opment of significant biological variables. The environmental variables such as altitude and slope were obtained from a digital elevation model, and NDVI was obtained from MODIS satellite images in August, 2014. This study evaluated the relationship between the num- ber of collected Ph. papatasi as the dependent variable and the independent variables. The data from the sampled villages were entered into ArcMap as a point layer, and each of the independent variables was entered into ArcMap as a raster layer. Then, each village layer was activated separately with an independent var- iable layer, by using spatial analyst tools and the value to point submenu, the numerical val- ue of each independent variable in a cell, where the selected village was located, was extracted and entered into SPSS 22.0. Eventually, due to the non-normal distribution of densities of Ph. papatasi and the lack of linear regression assumptions, the relationship between the den- sities of Ph. papatasi with the bioclimatic var- iables, the environmental variables, and NDVI was examined using Spearman's correlation test. Results In this study, a total of 1773 Ph. papatasi were collected from 34 villages of Golestan Province, with the highest frequency in Gon- bad-e-Kavus and Maraveh Tappeh counties (Table 1). The findings show that max tem- perature of warmest month (˚C), temperature an- http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 225–235 S H Hosseini et al.: The Effect of … 228 http://jad.tums.ac.ir Published Online: June 30, 2021 nual range (BIO5-BIO6) (˚C), temperature sea- sonality (±SD×100), mean diurnal range (aver- age min/max temp) (˚C), precipitation season- ality (coefficient of variation), mean temperature of driest quarter (˚C), and mean temperature of warmest quarter (˚C) were positively asso- ciated with the density of Ph. papatasi, More- over, the density of Ph. papatasi showed a positive inverse correlation with NDVI, but no correlation with altitude and slope (Table 2). Table 1. Densities of Phlebotomus papatasi in different counties of Golestan Province, 2014 County Number of se- lected villages Number of collected Ph. papatasi Number of collected Ph. papatasi for 60 traps Maraveh Tapeh 3 396 132 Gonbad-e Kavus 4 564 141 Aqqala 2 114 57 Ramiyan 2 42 21 Gomishan 2 64 32 Aliabad-e Katul 3 156 52 Azadshahr 3 138 46 Gorgan 2 14 7 Kalaleh 3 261 87 Kordkuy 2 2 1 Bandar-e Gaz 2 0 0 Bandar-e torkman 2 10 5 Galikesh 2 6 3 Minudasht 2 6 3 Total 34 1773 52.1 Table 2. Bioclimatic and environmental variables with direct and positive correlation with densities of Phlebotomus papatasi Correlation Variables Mean±SD* Correlation Coefficient P Direct and positive Number of collected Ph. papatasi 50.08±54.43 r= 0.747 P= 0.00 Max temperature of warmest month (°C) 34.06±1.16 Number of. collected Ph. papatasi 50.08±54.43 r= 0.529 P= 0.002 Temperature annual range (max temp of warmest month–min temp of coldest month) (°C) 32.01±2.17 Number of. collected Ph. papatasi 50.08±54.43 r= 0.523 P= 0.002 Temperature seasonality (standard deviation ×100) 7.66±0.56 Number of. collected Ph. papatasi 50.08±54.43 r= 0.466 P= 0.006 Mean diurnal range (mean of monthly (max temp–min temp)) (°C) 11.52±0.87 Number of. collected Ph. papatasi 50.08±54.43 r= 0.465 P= 0.006 Precipitation seasonality (coefficient of variation) 57.45±8.91 Number of. collected Ph. papatasi 50.08±54.43 r= 0.449 P= 0.009 Mean temperature of driest quarter (°C) 26.81±1.08 Number of. collected Ph. papatasi 50.08±54.43 r= 0.387 P= 0.026 Mean temperature of warmest quarter(°C) 26.97±0.87 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.345 P= 0.045 NDVI 0.36±0.11 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.459 P= 0.007 Annual precipitation (mm) 348.42±80.26 Number of. collected Ph. papatasi 50.08±54.43 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 225–235 S H Hosseini et al.: The Effect of … 229 http://jad.tums.ac.ir Published Online: June 30, 2021 Direct and negative Precipitation of driest month (mm) 6.78±4.41 r= - 0.497 P= 0.003 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.552 P= 0.001 Precipitation of driest quarter (mm) 23.93±13.56 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.590 P = 0.00 Precipitation of warmest quarter (mm) 25.66±13.29 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.348 P= 0.047 Precipitation of coldest quarter (mm) 120.6±22.66 Without correlation Number of. collected Ph. papatasi 50.08±54.43 r= 0.018 P= 0.925 Altitude 208.48±312.79 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.174 P= 0.331 Slope 89.78±0.37 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.127 P= 0.481 Annual mean temperature (°C) 17.20±1.15 Number of. collected Ph. papatasi 50.08±54.43 r= 0.123 P= 0.495 Isothermality (BIO2/BIO7) (×100) 3.54±0.09 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.244 P= 0.164 Mean temperature of wettest quarter (°C) 25.16±21.75 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.323 P= 0.067 Mean temperature of coldest quarter (°C) 7.60±1.88 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.285 P= 0.108 Precipitation of wettest month (mm) 60.06±13.27 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.191 P= 0.287 Precipitation of wettest quarter (mm) 145.15±25.53 Number of. collected Ph. papatasi 50.08±54.43 r= - 0.340 P= 0.053 Min temperature of coldest month (°C) 2.05±1.93 *: standard deviation !( !( !( !( !( !( !( !( !( !( !( !( !( !( !( !( !( !( !( !( !( !( !( !( !(!( !(!(!( !( !( !(!( !( Gonbad-e Kavus Aqqala Kalaleh Gorgan Maraveh Tappeh Gomishan Galikesh Kordkuy Ramiyan Azadshahr Minudasht Aliabad-e Katul Bandar-e Gaz Bandar-e Torkaman Legend !( selected villages Golestan Province Counties ¯ 0 30 60 90 12015 Kilometers Fig. 1. Location of Golestan Province in Iran and collection sites for Phlebotomus papatasi Table 2. Continued … http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 225–235 S H Hosseini et al.: The Effect of … 230 http://jad.tums.ac.ir Published Online: June 30, 2021 Discussion The highest frequency of the collected Ph. papatasi was reported in Gonbad-e-Kavus and Maraveh Tappeh counties in accordance with results of a similar study conducted in Golestan Province, similarly reporting that the presence probability of this species was higher in these counties (21). These two counties are known as endemic focus for CL in Golestan Province (4-9). Moreover, the incidence of CL and the number of the rodent’s active burrows (well- known reservoir hosts of ZCL) were higher in these regions than in the other regions of Go- lestan Province (7, 9, 15). Temperature was shown as one of the main factors associated with the growth and devel- opment of insects such as Ph. papatasi (19). The results of this study revealed that temper- ature significantly affected the density of Ph. papatasi. The densities of Ph. papatasi were significantly positively associated with factors such as max temperature of warmest month (°C), temperature annual range (BIO5-BIO6) (°C), temperature seasonality (standard devia- tion ×100), mean diurnal range (mean of max/ min temp) (°C), mean temperature of driest quarter (°C), and mean temperature of warmest quarter (°C). However, there was no signifi- cant relationship between the densities of Ph. papatasi with annual mean temperature (°C), isothermally (BIO2/BIO7) (×100), mean tem- perature of wettest quarter (°C), mean temper- ature of coldest quarter (°C), and min temper- ature of coldest month (°C). It can be concluded that max and mean temperatures of driest and warmest quarters and months were significantly associated with the density of Ph. papatasi. However, mean temperature of wettest and cold- est quarters and months had no significant role in the density of Ph. papatasi, which may be due to the effect of degree-day on the growth, development, and density of different species of insects. Degree-day is a measure of the amount of heat that accumulates above a spec- ified temperature during a 24h period (27). Ac cording to results of studies on the growth of this species, a specific temperature limit is re- quired for growth, and temperatures higher or lower than this limit will lead to a stop of growth. The maximum temperature threshold for the growth of this species is 35 °C, and the optimal minimum temperature for the growth according to different growth stages of this species is 20, 25, and 11.6 °C. As such, pre- oviposition activities are carried out at a tem- perature above 20 °C (8, 28-29). Therefore, temperature in the cold seasons, in which the air temperature does not reach 20 °C, cannot have a significant relationship with the den- sity of this species. Colacicco-Mayhugh MG et al. (23) found that max temperature of warm- est month was one of the most critical factors associated with the density of Ph. papatasi in Eastern Mediterranean, which is supported by the findings of our study. They also showed that mean temperature of coldest quarters and min temperature of coldest month were the most influential factors in the density of this spe- cies (23); while, in our study, there was no significant relationship between the values of these variables and the densities of Ph. papa- tasi. Further, the results of the present re- search showed no significant relationship be- tween the densities of Ph. papatasi with iso- thermality (BIO2/BIO7) (×100) and mean tem- perature of wettest quarter (°C). These varia- bles had low effects on the density of Ph. pa- patasi in another study conducted in Golestan Province (21). However, in a study conducted in Iran (22), contrary to the results of this study, isothermality (BIO2/BIO7) (×100) and mean temperature of wettest quarter (°C) showed high impacts on the density of this species. In addition, we found no significant relation- ship between annual mean temperature and den- sities of Ph. papatasi. This result is in accord- ance with the results of a study in Iran (22), showing a relatively low correlation between this factor and the density of Ph. papatasi. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 225–235 S H Hosseini et al.: The Effect of … 231 http://jad.tums.ac.ir Published Online: June 30, 2021 While in a study conducted in Golestan Prov- ince (21), this variable showed a significant effect on the density of this species. Differ- ences between the results of these studies and those of our study may be due to differences in the nature of these studies. All of these studies applied the MaxEnt Model as an ecological Niche model, in which modeling and predic- tion are based on the existence of a species in a region (30) and quantity is not measured. However, the present study analyzed the ef- fect of each variable quantity on the densities of Ph. papatasi and quantity had a direct ef- fect on the study outcomes. Precipitation was another main factor asso- ciated with the density of Ph. papatasi. The findings of the current study suggested that the densities of Ph. papatasi were positively associated with precipitation seasonality (co- efficient of variation). In other words, the in- creased precipitation increased the density of sand flies, which is in accordance with the re- sults of studies conducted in Iran and other countries (22, 31-32). Rainfall influences the dynamics, reproduction, and breeding of vec- tors such as sandflies (33-34), as sandflies need a certain amount of moisture for their devel- opment and survival. However, heavy rainfalls can kill adults and immature stages of sand flies (35-38). We found no significant relationship between the density of Ph. papatasi with precipitation of wettest quarter and precipitation of wettest month. However, Hanafi-bojd et al. (22) and Rodgers et al. (39) revealed that precipitation of wettest quarter was a major factor associ- ated with the density of Ph. papatasi. Colac- icco-Mayhugh MG et al. (23) revealed that precipitation of wettest quarter and precipita- tion of wettest month were not significantly associated with the abundance of Ph. papa- tasi, which is consistent with our study. Per- haps the reason for this is that the wettest months and quarters of the year occur in win- ter and sand flies have no activity in this sea- son; with the end of the wet months of the year, the population of sand flies increases, as it was pointed out in another article (40). Moreover, NDVI is another factor associ- ated with the density of Ph. papatasi. The find- ings of our study revealed a significant reverse relationship between NDVI and the densities of Ph. papatasi, as this species is more abun- dant in areas with lower NDVI, which is in compliance with other studies conducted in this province and in Morocco County (15, 21, 41). Moreover, Abdel-dayme et al. (20) showed vegetation type as a major factor associated with the density of Ph. papatasi. Colacicco-May- hugh MG (23) also introduced land cover as a significant factor associated with the density of Ph. papatasi. Moreover, Mollalo et al. (42) revealed a significant negative relationship be- tween NDVI and the incidence of ZCL, as ZCL is more prevalent in areas with lower NDVI. Therefore, it can be concluded that NDVI is an essential factor in the incidence of ZCL. Another factor associated with the density of Ph. papatasi is elevation. Accordingly, in a previous study conducted in Golestan Pro- vince, Ph. papatasi was collected at altitudes ranging from -32m from sea level to 598m above sea level, and densities of this species were more in plain areas with a lower altitude than in areas with a higher altitude (15). In a study conducted in Libya (20), it was ob- served that areas with an altitude lower than 600m were mostly suitable for the distribution of Ph. papatasi. Further, in a study conducted in Pakistan (43), altitude had the highest ef- fect on the density of CL among various ex- amined variables and Ph. papatasi was the do- minant species in areas with a higher altitude. However, in this study, there was no signi- ficant relationship between altitude and the abundance of Ph. papatasi, which is incon- sistent with previous studies. Regarding slope as another factor asso- ciated with the density of Ph. papatasi, in dif- ferent studies conducted in Golestan Province (21, 44) and Iran (22), slope was introduced as a major factor in the density of Ph. pa- http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 225–235 S H Hosseini et al.: The Effect of … 232 http://jad.tums.ac.ir Published Online: June 30, 2021 patasi. However, the findings of the present study showed no significant relationship bet- ween slope and the densities of Ph. papatasi. The density of sandflies might also depend on other environmental factors, such as soil type, land-use, or wind, which can impair their flight activity (38). In the present study, we could not assess the relationship between these factors and the density of Ph. papatasi, which could be one of the limitations of the study. Conclusions Air temperature and precipitation were shown as the most important factors in the density of Ph. papatasi in Golestan Province as the endemic focus of zoonotic cutaneous leishmaniasis in Iran. Acknowledgements This paper is part of a project approved by Infectious Diseases Research Center, Golestan University of Medical Sciences (grand No: 930708134). The authors would like to ex- press their sincere gratitude to all staff and supervisors of this center who provided finan- cial assistance and contributed to this thesis. The authors declare that they have no com- peting interests. References 1. Yaghoobi-Ershadi MR (2012) Phlebotom- ine sand flies (Diptera: Psychodidae) in Iran and their role on Leishmania trans- mission. J Arthropod Borne Dis. 6: 1–17. 2. 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