J Arthropod-Borne Dis, March 2020, 14(1): 17–28 M Daoudi et al.: Modeling Spatial Distribution of … 17 http://jad.tums.ac.ir Published Online: March 31, 2020 Original Article Modeling Spatial Distribution of Sergentomyia minuta (Diptera: Psychodidae) and Its Potential Implication in Leishmaniasis Transmission in Morocco Morocco Mohamed Daoudi1; *Samia Boussaa1,2; Ali Boumezzough1 1 Laboratory of Ecology and Environment (L2E), (URAC 32), Cadi Ayyad University, Faculty of Sciences Semlalia, Marrakesh, Morocco 2 ISPITS-Higher Institute of Nursing and Technical Health Occupations, Ministry of Health, Marrakesh, Morocco (Received 07 Aug 2018; accepted 07 Mar 2020) Abstract Background: Leishmaniases are parasitic diseases caused by Leishmania species and transmitted by the bite of sand flies. The genus Lutzomyia and Phlebotomus of sand flies are known to be the responsible vector for transmitting almost all Leishmania species to humans. The detection of Leishmania DNA in species of the genus Sergentomyia, in different regions, suggests their likely role in Leishmania transmission. Methods: Our objective was to determine the potential geographical distribution of Sergentomyia minuta, the most dominant Sergentomyia species in Morocco, using ecological niche modeling. Results: The results showed the widespread geographical distribution of S. minuta in Morocco, specifically in northern and central Morocco where visceral and cutaneous leishmaniasis foci occur. There were six abiotic factors affecting the distribution of S. minuta whose annual precipitation, precipitation seasonality and precipitation of driest month as the most important ecological variables of the model. Conclusion: A positive statistical correlation between human leishmaniasis cases and S. minuta abundance was noted suggesting the potential involvement of S. minuta in local Leishmania transmission cycles. Keywords: Sergentomyia minuta; Ecological niche modeling; Maximum entropy (MaxEnt); Morocco Introduction Phlebotomine sand flies (Diptera: Psychodi- dae) are small nocturnal insects of which only the female is a hematophagous. Currently, about 1000 species of sand flies are distributed in al- most all biogeographic regions of the world (1). These insects play a crucial role in the epidemi- ology of relevant diseases, some being of great veterinary and medical importance. Indeed, cer- tain species of sand flies are vectors of various infectious and parasitic agents such as agents of canine and human leishmaniasis, bartonello- sis and several arboviruses. Allergic reactions can also be caused by the exposure of sand fly bites, though is not linked to the spread of dis- ease (2). Leishmaniasis remains the most related dis- eases to sand flies. The genera Phlebotomus, Lutzomyia and Sergentomyia contain all hema tophagous species of sand flies (3), with only the genus Lutzomyia in the New World, and Phlebotomus in the Old World responsible for transmitting almost all Leishmania species to humans (4, 5). Like most countries around the Mediterra- nean, leishmaniases in Morocco are a serious public health problem. These affections are widely represented, from the Moroccan Rif Mountains to the palm groves of the Moroccan Anti-Atlas (6). Three epidemiological entities are known in Morocco: zoonotic cutaneous leish- maniasis due to Leishmania major, anthropon- otic cutaneous leishmaniasis due to L. tropica and visceral and cutaneous leishmaniasis due to L. infantum (6). Regarding disease transmission, only vecto- rial role of species of the genus Phlebotomus (namely, Phlebotomus papatasi, P. sergenti, P. ariasi, P. longicuspis and P. perniciosus) was *Corresponding author: Dr Samia Boussaa, E-mail: samiaboussaa@gmail.com http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 17–28 M Daoudi et al.: Modeling Spatial Distribution of … 18 http://jad.tums.ac.ir Published Online: March 31, 2020 investigated in Morocco (7–9); where sand fly fauna has 22 species including, nine species of the genus Sergentomyia (10): Sergentomyia christophersi, S. clydei, S. africana, S. minuta, S. dreyfussi, S. schwetzi, S. antennata, S. fallax and S. lewisi. Considering the epidemiological status of leishmaniasis in Morocco, it is critically im- portant to highlight the probable role as a vec- tor for other sand fly species. Vector incrimi- nation depends on the accumulation of evidence based mainly on its geographical and temporal abundance. According to many authors, Ser- gentomyia species are spread throughout Mo- rocco, especially S. minuta and S. fallax (11, 12). Sergentomyia minuta is collected in urban as well as in rural area (13) up to 1,200m (14). It was considered as ubiquitous species in Mo- rocco (15) with high density and a long activ- ity period (16, 17). In addition, Leishmania DNA was detected in species of the genus Sergentomyia in differ- ent regions suggesting their likely role in Leish- mania transmission (18). Studies conducted in leishmaniasis foci in Iran, Mali and Portugal have reported the detection of L. major DNA in Sergentomyia sintoni (19), S. darlingi (20) and S. minuta (21). Earlier, it has also been iso- lated from S. garnhami in Kenya (22). Other reports also detected L. donovani DNA in S. babu in India (23) and more recently, L. sia- mensis detected in S. gemmea in Thailand (24). Moreover, several viruses have been iso- lated from sand flies of the genus Sergentomyia such as the Saboya virus, viruses RNA of ArD 95737 and ArD 111740 (25, 26), which has made it possible to suspect the vector role of Sergentomyia species (27). Despite the presence and the abundance of Sergentomyia species in Morocco, no study has invested its potential involvement in leishman- iasis transmission cycles. Therefore, we used ecological niche modeling to identify the dis- tribution of the most dominant species of Ser- gentomyia genus in Morocco and consequently discuss its potential involvement in local Leish- mania transmission cycles. Materials and Methods Study area Morocco is a northern African country, bor- dering the North Atlantic Ocean and the Medi- terranean Sea. The current study covered sand fly sampling in 190 localities with altitude rang- es between sea level and up to 2123m above sea (Fig. 1). These localities covered mainly northern and central Morocco, where human cutaneous and visceral leishmaniases are endem- ic (28). The climate in Morocco is mostly Mediter- ranean; however, seven bioclimatic regimes are occurred due to topographic differences across the country (Fig. 1). In 2014, the total human population in Morocco is about 33.7 million, with an urbanization rate of 60% (29). Occurrence data and environmental variables Occurrence records of sand flies were col- lected from our field survey (published and un- published data) and literature using the key- word “species name, Morocco” as a search word to retrieve all data archived in PubMed data- base. Thus, about 70% of the 190 localities were investigated by the Ecology and Environment Laboratory (L2E) team between 2005 and 2016. The rest of the localities were published ob- servations of the investigations in Morocco (20 publications on PUBMED). The coordinates of all localities were registered with a global po- sitioning system (GPS). For ecological niche modeling, 19 climatic variables (Bio1-Bio19) were used with eleva- tion precision (ALT) for each locality (Table 1). Altitude and bioclimatic data were ob- tained from the WorldClim project (http://www.worldclim.org), with a spatial res- olution of 30 arc seconds (about 1km2). Construction of the model The modeling was performed using Maxi- mum entropy (MaxEnt) version 3.3.3 (30), which http://jad.tums.ac.ir/ http://www.worldclim.org/ J Arthropod-Borne Dis, March 2020, 14(1): 17–28 M Daoudi et al.: Modeling Spatial Distribution of … 19 http://jad.tums.ac.ir Published Online: March 31, 2020 uses an optimization procedure comparing the presence of the species with the characteristics of the environment, based on the principle of maximum entropy. This program allows for in- ference from incomplete information despite limited occurrence data (31–33). Distribution data for the sand fly species and environmental data were imported into MaxEnt v. 3. 3. 3 (31), a total of 15 model replicates were run, with 30% of the points of presence used to test the model and 70% for model construc- tion (34). Model Evaluation To evaluate the quality of model produced by MaxEnt, we analyzed the Operating Char- acteristics Curve Receiver Operating Charac- teristic (ROC) which assigns a unique value ac- cording to the model performance Area Under the Curve (AUC). ROC analysis is a measure of sensitivity, which corresponds to the true positive rate (no error of omission), compared to the false posi- tive rate (superfluous forecast error). Also, the ROC analysis evaluates the ability of the model to correctly predict the occurrence of the spe- cies. The closer the AUC value is to 1, the clos- er the correlation of the model (31) (Figs. 2, 3). The importance of the variables in explaining the potential geographic distribution of S. minu- ta was estimated using the Jackknife Environ- mental Variables Importance Test (31) (Table 2), which assesses the relative contribution (%) of the variables used to generate the distribu- tion model produced by MaxEnt. Statistical analysis The Chi-squared test (𝜒2) was used to ana- lyze the correlation between variation of S. minu- ta abundance and the presence/absence of hu- man leishmaniasis cases (cutaneous leishman- iasis by L. tropica and visceral leishmaniasis by L. infantum) in all sampling sites. Epidemiological data (human cutaneous and visceral leishmaniasis cases) were obtained from official Moroccan Ministry of Health reports (28). Results In this study, we assembled 190 sampling sites for sand fly species. Five Sergentomyia species were noted: Sergentomyia minuta (N= 150), S. fallax (N= 110), S. dreyfussi (N= 57), S. africana (N= 10) and S. christophersi (N= 15). Phlebotomus species were also recorded, spe- cifically Phlebotomus sergenti (N= 102), P. pa- patasi (N= 82), P. longicuspis (N= 78), P. per- niciosus (N= 76) and P. ariasi (N= 43), while P. alexandri (N= 09), P. kazeruni (N= 03), P. langeroni (N= 02), and P. mariae (N= 02) were noted with very low reporting. Sergentomyia minuta was the most predomi- nant species and it was collected in the 150/ 190 sampling sites between 14 and 2123m (Ta- ble 3). To identify habitat suitability and poten- tial limiting factor of S. minuta, all ecological variables were analyzed. There were 6/19 eco- logical variables (Bio 3, Bio 4, Bio 12, Bio 14, Bio 15, Bio 19), which were the most important factors affecting the distribution of S. minuta in the study area. Figure 4 shows a representation of the MaxEnt model for the S. minuta. Warmer col- ors show areas with better predicted condi- tions. The white dots indicate the presence lo- cations used for training, while the purple dots show the locations of the tests. Since 1995, leishmaniases are notifiable dis- eases in Morocco (Ministerial decree n°683-95). All human cases are listed in leishmaniasis epi- demiological information collection system and published yearly. We used data recorded of CL and VL between 2005 and 2016 (28) corre- sponding to 190 localities. Statistical analysis of the presence and ab- sence of leishmaniasis cases (cutaneous CL and visceral leishmaniasis VL) and the distribution of S. minuta in Morocco showed a positive cor- relation between VL by L. infantum and S. minu- ta abundance (r= 0.211) and between CL by L. tropica and S. minuta abundance (r= 0.166). According to Chi-squared test (𝜒2) test, S. minuta was more associated to VL distribution http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 17–28 M Daoudi et al.: Modeling Spatial Distribution of … 20 http://jad.tums.ac.ir Published Online: March 31, 2020 (𝜒2= 7,166, ddl= 2, P= 0,028) compared to CL (𝜒2= 3,256, ddl= 2, P= 0,196). Table 1. Description and sources of environmental variables collected for the model Environmental variables Abbreviation Unit Source Annual mean temperature Bio 1 °C WorldClim Mean diurnal range (mean of monthly (max tem- perature−min temperature)) Bio 2 °C WorldClim Isothermality (BIO2/BIO7) (×100) Bio 3 _ WorldClim Temperature seasonality (standard deviation ×100) Bio 4 °C WorldClim Max temperature of warmest month Bio 5 °C WorldClim Min temperature of coldest month Bio 6 °C WorldClim Temperature annual range (BIO5–BIO6) Bio 7 °C WorldClim Mean temperature of wettest quarter Bio 8 °C WorldClim Mean temperature of driest quarter Bio 9 °C WorldClim Mean temperature of warmest quarter Bio 10 °C WorldClim Mean temperature of coldest quarter Bio 11 °C WorldClim Annual precipitation Bio 12 mm WorldClim Precipitation of wettest month Bio 13 mm WorldClim Precipitation of driest month Bio 14 mm WorldClim Precipitation seasonality (coefficient of variation) Bio 15 mm WorldClim Precipitation of wettest quarter Bio 16 mm WorldClim Precipitation of driest quarter Bio 17 mm WorldClim Precipitation of warmest quarter Bio 18 mm WorldClim Precipitation of coldest quarter Bio 19 mm WorldClim Elevation ALT m GTOPO30 Fig. 1. Distribution of the Sergentomyia spp in Morocco according to bioclimate map http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 17–28 M Daoudi et al.: Modeling Spatial Distribution of … 21 http://jad.tums.ac.ir Published Online: March 31, 2020 Table 2. Analysis of the contribution of the most important ecological variables of the model Variable Percent contribution (%) AUC without the variable AUC with only the variable Bio 12 41.2 0.917 0.867 Bio 15 23.9 0.922 0.892 Bio 14 9.4 0.916 0.859 Bio 4 5.9 0.914 0.890 Bio 19 5.5 0.914 0.906 Bio 3 4.8 0.914 0.868 Table 3. Description of Sergentomyia species on sampling sites Sergentomyia spp. Total of specimens Number of stations occupied Altitude range (m) S. minuta 6746 150 [14–2123] S. fallax 5582 110 [14–1351] S. dreyfussi 474 57 [282–1309] S. africana 43 10 [402–1340] S. christophersi 99 15 [282–1500] Fig. 2. Analysis of the omission / commission of Sergentomyia minuta http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 17–28 M Daoudi et al.: Modeling Spatial Distribution of … 22 http://jad.tums.ac.ir Published Online: March 31, 2020 Fig. 3. Sensitivity and performance of the model for Sergentomyia minuta species Fig. 4. Estimation of the distribution of Sergentomyia minuta species in Morocco by MaxEnt Discussion Morocco is located in the subtropical zone. It benefits from a Mediterranean climate, charac- terized by a dry warm season, nuanced by three essential influences: the progressive remoteness of the Atlantic coast, the altitude and the ap- proach of the southern desert (36). The geo- graphical location of Morocco is a major fac- tor of its bioclimatic diversity which favors the abundance and the diversity of phlebotomine species; including Sergentomyia species that can tolerate the aridity (37-39). Thus, a consid- erable specific richness in Morocco for Ser- gentomyia genus counter to the others Medi- terranean’s regions such as Tunisia, where on- ly six species of Sergentomyia have been re- ported (40-42). Sergentomyia species were collected in dif- ferent environments but are rather subservient to the extradomestic environment (43). This is related to their trophic preferences, and their adaptability to dry and open habitats. Thus, they find suitable conditions in wild environments. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 17–28 M Daoudi et al.: Modeling Spatial Distribution of … 23 http://jad.tums.ac.ir Published Online: March 31, 2020 According to WHO (43), sand flies of the genus Sergentomyia have long been known to feed on reptiles. They are involved in the transmission of Sauroleishmania, of reptiles in the Old World. They do not present an epide- miological risk for humans (44), although some species can feed on humans (45). Recent work on Sergentomyia spp shows that these species can be infected by human Leishmania spp. and the blood meal analysis shows that it is a mammalian blood, including humans (18). Leishmania tropica DNA was detected from S. ingrami and S. hamoni collected in Ghana (46). All of these results raise questions about the role of Sergentomyia spp. as a possible vector of Leishmania spp. which has a great impact on human and animal health. Among all Sergentomyia species, S. minuta is widely distributed around the Mediterrane- an area. It is the most abundant Sergentomyia species in the present study (Table 3) and ear- ly in Morocco (12). In Greece, the Sergentomyia genus repre- sented 84% of the total sand flies fauna with 38% of S. minuta (47). In France, Rioux et al. (48) reported a percentage of 73.7% for both genus and species. In Tunisia, it was noted that Sergentomyia accounted for 70% of sand flies, of which 41.5% belonged to the species S. minu- ta (49). In Algeria, Belazzoug et al. (50) found this species with a rate of 39.75% of total spec- imens. Regarding its potential vector role, Periera et al. (51) have isolated L. infantum from S. minuta, and blood meal analysis has shown that it is human blood. In Italy, recently, Latrofa et al. (52) detected L. infantum DNA in S. minuta from endemic area of canine leishmaniasis. S. minuta was also naturally infected with L. ma- jor in Portugal (21) and in Tunisia (53). In ad- dition, Maia et al. (54) detected Leishmania spp. in S. minuta collected in southern Portugal; while Bravo-Barriga et al. (55) identified Leishmania DNA in S. minuta of Spain. In Morocco, though the well-known role of Phlebotomus papatasi, P. sergenti and Larrous- sius species (P. perniciosus, P. longicuspis and P. ariasi), as competent vector of L. major, L. tropica and L. infantum, respectively (56), that of S. minuta needs further investigation. Ecological niche modelling has been wide- ly used in order to identify the probability of sand fly species occurrence (57). To the best of our knowledge, the present study constitutes a first modeling of Sergentomyia species. AUC values of our model were greater than 0.9 (Ta- ble 2) indicating that the model performed has a good robustness (31). In the 190 localities used for the model, we noted the coexistence of Sergentomyia species and Phlebotomus species including the proven vectors of leishmaniasis forms in Morocco: P. papatasi, P. sergenti, P. perniciosus, P. ariasi and P. longicuspis. According to the region, P. sergenti and P. papatasi were more abundant in the central Morocco, while P. perniciosus was more recorded in northern Morocco. The presence and the abundance of S. minuta in the endemic area of leishmaniasis in Moroc- co can be the most important criteria for its pos- sible vectorial incrimination. Our results showed the widespread geographical distribution of S. minuta in Morocco, specifically in northern and central Morocco (Fig. 4) where VL and CL foci occur (16, 58). In addition, a positive correlation between visceral leishmaniasis (r= 0.211) and cutaneous leishmaniasis (r= 0.166) with S. minuta abun- dance was noted and confirm this S. minuta- Leishmania spatial overlapping. Sand fly behaviors can also determine its vector implication. S. minuta presented an an- thropophilic behavior in Portugal (54). In Mo- rocco, S. minuta is a ubiquitous species (13) which shows an adaptation and an important ecological tolerance. It was collected in the different bioclimatic floors with preference to a semiarid climate and altitudes between 800 to 1,000m (12). In addition, the seasonal dis- tribution of S. minuta showed abundance from May to September in sub-humid and semi-arid stages in Morocco (15). In arid bioclimate, it http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 17–28 M Daoudi et al.: Modeling Spatial Distribution of … 24 http://jad.tums.ac.ir Published Online: March 31, 2020 was active during two periods, October–No- vember and April–May–June (59). This long pe- riod of S. minuta activity favors the S. minuta- Leishmania temporal overlapping in these areas. Sand flies of Morocco, including Sergento- myia species, were found highly dependent on environmental conditions; and their abundance and geographical distribution were affected by several ecological variables (59-62). According to our model, annual precipitation (Bio 12) and precipitation seasonality (Bio 15) were signif- icantly more important in the distribution of S. minuta in Morocco (Table 2). Precipitation plays an important role in sand flies’ life cy- cle (63). Modeling approach of Chargaff et al. (57), found that annual precipitation has a significant role in distribution of Leishmania vector species in Mediterranean basin (57). S. minuta is recorded in arid region of Tu- nisia with an annual precipitation between 88 and 157mm (53), also in Portugal with an an- nual precipitation equal to 730mm (64). In the present study, it prefers regions with an annual precipitation (Bio 12) between: 50–1100mm, and precipitation seasonality (Bio 15) between: 30–100mm (Supporting Information S1). Conclusion Effective vector control requires accurate vector identification. The spatial and temporal overlapping of S. minuta with Leishmania spe- cies seemed to present the important criteria nec- essary to be incriminated as a potential vector of the Leishmania species in Morocco. Hence, the present study opened a debate on the po- tential role of Sergentomyia species, especial- ly S. minuta in the transmission of leishmania- sis in Morocco. 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