Modeling Spatial Distribution of Sergentomyia minuta (Diptera: Psychodidae) and its Potential Implication in Leishmaniasis Transmission in Morocco

  • Morocco Mohamed Daoudi Laboratory of Ecology and Environment (L2E), (URAC 32), Cadi Ayyad University, Faculty of Sciences Semlalia, Marrakesh, Morocco
  • Samia Boussaa Laboratory of Ecology and Environment (L2E), (URAC 32), Cadi Ayyad University, Faculty of Sciences Semlalia, Marrakesh, Morocco, ISPITS-Higher Institute of Nursing and Technical Health Occupations, Ministry of Health, Marrakesh, Morocco
  • Ali Boumezzough Laboratory of Ecology and Environment (L2E), (URAC 32), Cadi Ayyad University, Faculty of Sciences Semlalia, Marrakesh, Morocco
Sergentomyia minuta; Ecological niche modeling; MaxEnt; Morocco


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.


1. Hazratian T, Vatandoost H, Oshaghi MA, Yaghoobi-Ershadi MR, Fallah E, Rafiza-deh S, Shirzadi MR, Shayeghi M, Akbarza¬deh K, Rassi Y (2016) Diversity of sand flies (Dip¬tera: Psychodidae) in endemic focus of vis¬ceral leishmaniasis in Azar Shahr Dis¬trict, East Azarbaijan Province, north west of Iran. J Arthropod Borne Dis. 10(3): 328–334.
2. Belkaid Y, Valenzuela JG, Kamhawi S, Row¬ton E, Sacks DL, Ribeiro JM (2000) De¬layed-type hypersensitivity to Phlebotomus papatasi sand fly bite: An adaptive re¬sponse induced by the fly?. Proc Natl Acad Sci USA. 97(12): 6704–6709.
3. Killick-Kendrick R, Killick-Kendrick M (1999) Biology of sand fly vectors of Med¬i¬terranean canine leishmaniasis. In: Canine Leishmaniasis: an update. The First Inter¬na¬tional Canine Leishmaniasis Forum, 1999 February, Barcelona, Spain, pp. 28–31.
4. Mukherjee S, Hassan MQ, Ghosh A, Ghosh KN, Bhattacharya A, Adhya S (1997) Leish¬mania DNA in Phlebotomus and Sergento¬myia species during a kala-azar epidemic. Am J Trop Med Hyg. 57: 423–425.
5. Berdjane-Brouk Z, Koné AK, Djimde AA, Charrel RN, Ravel C, Delaunay P, del Giu¬dice P, Diarra AZ, Doumbo S, Goita S, Thera MA, Depaquit J, Marty P, Doumbo OK, Izri A (2012) First detection of Leish¬mania major DNA in Sergentomyia (Spelaeomyia) darlingi from cutaneous leish¬man¬iasis foci in Mali. PLoS One. 7: e28266.
6. Kahime K, Boussaa S, Bounoua L, Ouanai-mi F, Messouli M, Boumezzough A (2014) Leishmaniasis in Morocco: dis-eases and vectors. Asian Pac J Trop Dis. 4: 530–534.
7. Rioux JA, Guilvard E, Dereure J, Lanotte G, Denial M, Pratlong F, Serres E, Bel-monte A (1986) Infestation naturelle de Phle¬botomus papatasi (Scopoli, 1786) par Leishmania major MON-25. A propos de 28 souches iso¬lées dans un foyer du Sud Marocain. In Rioux J.A. (ed.) Leishma-nia. Taxinomie et phyloge¬nèse. Applica-tions écoépidémiologiques. In¬ternational Collo¬quium CNRS/INSERM, 1984 July 2–6. Ins¬titut Méditerranéen d’Etudes Épidémiolo¬giques et Ecologiques, Montpellier, France, pp. 471–480.
8. Ajaoud M, Es-sette N, Charrel RN, laamrani-Idrissi A, Nhammi H, Riyad M, Lemrani M (2015) Phlebotomus sergenti in a cutaneous leishmaniasis focus in Azilal Province (High Atlas, Morocco): Molecular detec¬tion and genotyping of Leishmania trop¬ica and feeding behavior. PLoS Negl Trop Dis. 9: e0003687.
9. Zarrouk A, Kahime K, Boussaa S, Belqat B (2015) Ecological and epidemiological sta¬tus of species of the Phlebotomus perni¬ciosus complex (Diptera: Psychodidae, Phlebotom¬inae) in Morocco. Parasitol Res. 115(3): 1045–1051.
10. Moroccan Ministry of Health (2010) Fight against Leishmaniasis. Activity Guide. Di¬rectorate of Epidemiology and Disease Con¬trol, Parasitic Diseases Service, Min-istry of Health. Morocco. Available at:
11. Ouanaimi F, Boussaa S, Boumezzough (2015) Phlebotomine sand flies (Diptera: Psy¬chodidae) of Morocco: results of an en¬tomo¬logical survey along three transects from northern to southern country. Asian Pac J Trop Dis. 5(4): 299–306.
12. Kahime K, Boussaa S, El Mazabi A, Bou-mezzough A (2015) Spatial relations be-tween Environmental factors and Phlebotom¬ine sand fly populations (Dip-tera: Psychodidae) in central and southern Mo¬rocco. J Vector Ecol. 40: 1–13.
13. Boussaa S, Boumezzough A, Sibold B, Alves-Pires C, Morillas Marquez F, Glass-er N, Pesson B (2009) Phlebotomine sand¬flies (Diptera: Psychodidae) of the genus Ser¬gentomyia in Marrakech region, Mo¬rocco. Parasitol Res. 104: 1027–1033.
14. Guernaoui S, Boumezzough A, Laamrani A
(2006) Altitudinal structuring of sandflies (Diptera: Psychodidae) in the High-Atlas moun¬tains (Morocco) and its relation to the risk of leishmaniasis transmission. Acta Trop. 97: 346–351.
15. Bailly-Choumara H, Abonnenc E, Pastre J (1971) Contribution à l’étude des phlébo-tomes du Maroc. (Diptera: Psychodidae): données faunistiques et écologiques. Cah ORSTOM. Ser Entomol Med Parasitol. 9: 431–460.
16. Boussaa S, Guernaoui S, Pesson B, Bou-mezzough A (2005) Seasonal fluctuations of phlebotomine sand fly populations (Dip¬tera: Psychodidae) in the urban area of Mar¬rakech, Morocco. Acta Trop. 95: 86–91.
17. El Miri H, Rhajaoui M, Himmi O, Oua¬habi S, Benhoussa A, Faraj C (2013) Ento¬mo-logical study of five cutaneous leishman-ia¬sis foci in the Sidi Kacem Province, north Morocco. Ann Soc Entomol Fr. 49(2): 154–159.
18. Maia C, Depaquit J (2016) Can Sergento-myia (Diptera: Psychodidae) play a role in the transmission of mammal-infecting Leishma¬nia? Parasite. 23: 55.
19. Parvizi P, Amirkhani A (2008) Mitochon-drial DNA characterization of Sergento-myia sintoni populations and finding mam¬malian Leishmania infections in this sand fly by us¬ing ITSrDNA. Iran J Vet Res. 22: 9–18.
20. Berdjane-Brouk Z, Koné AK, Djimde AA, Charrel RN, Ravel C, Delaunay P, del Giu¬dice, P, Diarra AZ, Doumbo S, Goita S, Thera MA, Depaquit J, Marty P, Doumbo OK, Izri A (2012) First detection of Leish¬ma¬nia major DNA in Sergentomyia (Spelaeo¬myia) darlingi from cutaneous leish¬man¬iasis foci in Mali. PLoS One. 7: e28266.
21. Campino L, Cortes S, Dionísio L, Neto L, Afonso MO, Maia C (2013) The first de-tec¬tion of Leishmania major in naturally infected Sergentomyia minuta in Portugal. Mem Inst Oswaldo Cruz. 108: 516–518.
22. Mutinga MJ, Massamba NN, Basimike M,
Kamau CC, Amimo FA, Onyido AE, Omo- go DM, Kyai FM, Wachira DW (1994) Cutane¬ous leishmaniasis in Kenya: Sergento¬myia garnhami (Diptera: Psychodidae), a possible vector of Leishmania major in Kitui District: a new focus of the disease. East Afr Med J. 71: 424–428.
23. Mukherjee S, Hassan MQ, Ghosh A, Ghosh KN, Bhattacharya A, Adhya S (1997) Leish¬mania DNA in Phlebotomus and Ser¬gento¬myia species during a kala-azar epi¬demic. Am J Trop Med Hyg. 57: 423–425.
24. Kanjanopas K, Siripattanapipong S, Ninsaeng U, Hitakarun A, Jitkaew S, Kaew¬taphaya P, Tan-ariya P, Mungthin M, Char¬oen¬wong C, Leelayoova S (2013) Sergento¬myia (Ne¬o¬phlebotomus) gem¬mea, a potential vector of Leishmania si-amensis in southern Thai¬land. BMC In-fect Dis. 13: 333.
25. Ba Y, Trouillet J, Thonnon J, Fontenille D (1999) Phlebotomus of Senegal: survey of the fauna in the region of Kedougou. Iso-lation of arbovirus. Bull Soc Pathol Exot. 92(2): 131–135.
26. Charrel RN, Izri A, Temmam S, de Lam-ballerie X, Parola P (2006) Toscana Virus RNA in Sergentomyia minuta Flies. Emerg Infect Dis. 12(8): 1299–1300.
27. Geevarghese G, Arankalle VA, Jadi R, Kanojia PC, Joshi MV, Mishra AC (2005) Detection of Chandipura virus from sand flies in the genus Sergento¬myia (Diptera: Phlebotomidae) at Ka¬rimnagar District, An¬dhra Pradesh, India. J Med Entomol. 42: 495–496.
28. Kholoud K, Denis S, Lahouari B, Ab¬del-monaim M, Hidan EJ, Soua B (2018) Man¬agement of Leishmaniases in the Era of Climate Change in Mo¬rocco. Int J En-viron Res Public Health. 15(7): 1542–1547.
29. High Planning Commission of Morocco (2014) Report of General Census of Pop-ula¬tion and Housing. Morocco. Available at:
30. Hijmans R, Cameron S, Parra J, Jones P, Jarvis A, Richardson K (2005) World-Clim, Version 1.3. University of Califor-nia, Berke¬ley.
31. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of spe¬cies geographic distributions. Ecol Modell. 190: 231–259.
32. Elith J, Graham CH, Anderson RP, Dudík M, Ferrier S, Guisan A, Hijmans RJ, Huett¬mann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, McC J, Over¬ton M, Townsend Peterson A, Phil¬lips SJ, Richardson K, Sca-chetti‐Pereira R, Schapire RE, Soberón J, Williams S, Wisz MS, Zim¬mermann NE (2006) Novel meth¬ods improve predic¬tion of species distributions from occur¬rence data. Ecography. 29: 129–151.
33. Pearson TRH, Brown SL, Birdsey RA (2007) Measurement guidelines for the se-questration of forest carbon Gen. Tech. Rep. NRS-18. Newtown Square, PA: U.S. Depart¬ment of Agriculture, Forest Service, Northern Research Station. p. 42.
34. Nogués-Bravo D (2009) Predicting the past distribution of species climatic nich-es. Glob Ecol Biogeogr. pp. 521–531.
35. Mokhtari N, Mrabet R, Lebailly P, Bock L (2014) Spatialisation des bioclimats, de l’aridité et des étages de végétation du Ma¬roc. Rev Mar Sci Agron Vét. 2(1): 50–66.
36. Sebbar A (2013) Etude de la variabilité et de l’évolution de la pluviométrie au Ma-roc (1935–2005): Réactualisation de la carte des précipitations. [PhD disserta-tion]. Faculté des Sciences Ben M’Sik Casablanca, Morocco.
37. Adler S, Theodor O (1929) The distribu-tion of sandflies and leishmaniasis in Pal-es¬tine, Syria and Mesopotamia. Ann Trop Med Parasitol. 23: 269–306.
38. Lupasco G, Duport M, Dancesco P, Cristes¬co A (1965) Recherches sur les es-pèces de Phlébotomes sauvages de Rou-manie. Arch Roum Pathol Exp Microbiol. 24: 195–202.
39. Newstead R, Sinton JA (1921) On a col-lec¬tion of Pappataci flies (Phlebotomus) from India. Ann Trop Med Parasitol. 15: 103–106.
40. Depaquit J, Léger N, Killick-Kendrick R (1998) Description de Phlebotomus (Pa-raphlebotomus) riouxi n. sp (Dip¬tera: Psy-chodidae) d’Afrique du Nord. Pa¬ra¬site. 151–158.
41. Ghrab J, Rhim A, Bach-Hamba D, Chahed MK, Aoun K, Nouira S, Bourat-bine A (2006) Phlebotominae (Diptera: Psychodi¬dae) of human leishmaniosis sites in Tu¬nisia. Parasite. 13 : 23–33.
42. Chamkhi J, Guerbouj S, Ben Ismail R, Guizani I (2006) Description of the hith-erto unknown female of Phlebotomus (Lar¬roussius) Chadlii, Rioux, Juminer and Gibily, 1966 (Diptera: Psychodidae). Par-asite. 13 (4): 299–303.
43. World Health Organization (2002) Ur¬ban-ization: an increasing risk factor for leish-maniasis. Wkly Epidemiol Rec. 77: 365–372.
44. Lane RP (1993) Sandflies (Phlebotom-inae). In: Lane, RP and Crosskey, RW (Eds.), Medical insects and arachids. (1st. Edn.), London, Chapman and Hall. pp. 78–119.
45. Hoogstraal H, Dietlein DR, Heyneman D (1962) Leishmaniasis in the Sudan Re-pub¬lic. Preliminary observations on man-bit¬ing sand¬flies (Psychodiae: Phleboto-mus) in cer¬tain Upper Nile endemic Nile endemic ar¬eas. Trans R Soc Trop Med Hyg. 411–422.
46. Nzelu CO, Kato H, Puplampu N, Desewu K, Odoom S, Wilson MD, Sakurai T, Kataku¬ra K, Boakye DA (2014) First de-tec¬tion of Leishmania tropica DNA and Trypa¬nosoma species in Sergentomyia sand flies (Diptera: Psychodidae) from an outbreak area of cutaneous leishmaniasis in Ghana. PLoS Negl Trop Dis. 8(2): 1–9.
47. Madulo-leblond G (1983) Les phlébo-tomes (Diptera: Phlebotomidae) des îles Io¬niennes. [PhD dissertation]. Université de Reins, France.
48. Rioux JA, Lanotte G, Petter F, Dereure J, Akalay O, Pratlong F, Velez ID, Fikri NB, Maazoum R, Denial M, Jarry DM, Zahaf A, Ashford RW, Cadi-Soussi M, Killick-Kendrick R, Benmansour N, Moreno G, Peri¬eres J, Guilvard E, Zribi M, Kennou MF, Rispail P, Knechtli E, Serres E (1986) Les leishmanioses cuta-nées du bassin mé¬diterra¬néen occidental: de l’identification enzy¬matique à l’analyse éco -épidemi¬ologique, l’exemple de trois ‘foyers’, tu¬nisien, marocain et français. In: Leishma¬nia. Taxonomie et Phylogenèse. Applica¬tions Écoépidémiolo¬giques, ed. Rioux, J.A. Montpellier, France: Institut Méditerra-néen d’Etudes Épidémiolo¬giques et Eco-lo¬giques. pp. 365–395.
49. Haddad N (1998) Les phlébotomes du Li-ban-Inventaire et corollaire éco- épi-démio¬logique. Université de Pharmacie Reims, France.
50. Belazzoug S, Mahzoul D, Rioux JA (1986) Les phlébotomes (Diptera: Psy-chodi¬dae) de M’sila et Bou-Saada. Ar-chives de l’Institut Pasteur Algérie. 55: 117–124.
51. Peira S, Pita-Pereira D, Araujo-Pereira T, Britto C, Costa-Rego T, Ferrolho J, Vilhe-na M, Rangel EF, Vilela ML, Afonso MO (2017) First molecular de¬tection of Leish-mania in¬fantum in Ser¬gentomyia minuta (Diptera: Psy¬chodidae) in Alentejo, sou-thern Portugal. Acta Trop. 174 : 45–48.
52. Latrofa MS, Iatta R, Dantas-Torres F, An-noscia G, Gabrielli S, Pombi M, Gradoni L, Otranto D (2018) Detection of Leish-mania infantum DNA in phlebotomine sand flies from an area where canine leishmaniosis is endemic in southern Italy. Vet Parasitol. 253: 39–42.
53. Jaouadi K, Ghawar W, Salem S, Gharbi M, Bettaieb J, Yazidi R, Harrabi M, Hamarsheh O, Ben Salah A (2015) First re¬port of naturally infected Sergentomyia minuta with Leishmania major in Tuni¬sia. Parasit Vectors. 8: 649.
54. Maia C, Parreira R, Cristóvão JM, Freitas
FB, Afonso MO, Campino L (2015) Mo-lecu¬lar detection of Leishmania DNA and identi¬fication of blood meals in wild caught phlebotomine sand flies (Diptera: Psycho¬di¬dae) from southern Portugal. Pa-rasit Vectors. 8: 173.
55. Bravo-Barriga D, Parreira R, Maia C, Blan¬co-Ciudad J, Odete AM, Frontera E, Campino L, Pérez-Martín JE, Serrano Aguilera FJ, Reina D (2016) First molec-ular detection of Leishmania tarentolae-like DNA in Sergentomyia minuta in Spain. Parasitol Res. 115: 1339.
56. Mhaidi I, El Kacem S, Ait Kbaich M, El Hamouchi A, Sarih M, Akarid K, Lemra-ni M (2018) Molecular identifica¬tion of Leishma¬nia infection in the most relevant sand fly species and in patient skin sam-ples from a cutaneous leish¬maniasis focus, in Morocco. PLoS Negl Trop Dis. 12(3): e0006315.
57. Chalghaf B, Chemkhi J, Mayala B, Har-rabi M, Benie GB, Michael E, Ben Salah A (2018) Ecological niche modeling pre-dicting the potential distribution of Leish-mania vec¬tors in the Mediterranean basin: impact of climate change. Parasit Vectors. 11(1): 461.
58. Rhajaoui M (2011) Human leishmaniases in Morocco. A nosogeographical diver-sity. Pathol Bio. 59(4): 226–229.
59. Rioux JA, Rispail P, Lanotte G, Lepart J (1984) Relations Phlébotomes-bioclimats en écologie des leishmanioses Corollaires épi¬démiologiques. L’exemple du Maroc. Bull Soc Bot. France. 131(2–4): 549–557.
60. Rispail P, Dereure J, Jarry D (2002) Risk zones of human Leishmaniases in the West¬ern Mediterranean basin: correla¬tions between vector sand flies, biocli¬matology and phyto¬sociology. Mem Inst Oswaldo Cruz. 97(4): 477–483.
61. Bounoua L, Kahime K, Houti L, Blakey T, Ebi KL, Zhang P, Imhoff ML, Thome KJ, Dudek C, Sahabi SA, Messouli M, Makhlouf B, El Laamrani A, Boumez-zough A (2013) Linking climate to inci-dence of zoonotic cu¬taneous leishmania¬sis (L. major) in pre-Sa¬haran North Af¬rica. Int J En¬viron Res Public Health. 10(8): 3172–3191.
62. Boussaa S, Kahime K, Samy AM, Salem AB, Boumezzough A (2016) Species com¬po¬sition of sand flies and bionomics of Phlebotomus papatasi and P. sergenti (Dip¬tera: Psychodidae) in cutaneous leishmaniasis endemic foci, Morocco. Parasit Vectors. 9: 60.
63. Kasap OE, Alten B (2006) Comparative demography of the sand fly Phlebotomus pa¬patasi (Diptera: Psychodidae) at con-stant temperatures. J Vector Ecol. 31: 378–385.
64. Branco S, Alves-Pires C, Maia C, Cortes S, Cristovão JMS, Gonçalves L, Campino L, Afonso MO (2013) Entomological and eco¬logical studies in a new potential zo-onotic leishmaniasis focus in Torres No-vas munici¬pality, Central Region, Portu-gal. Acta Trop. 125(3): 339–348.
How to Cite
Daoudi MM, Boussaa S, Boumezzough A. Modeling Spatial Distribution of Sergentomyia minuta (Diptera: Psychodidae) and its Potential Implication in Leishmaniasis Transmission in Morocco. J Arthropod Borne Dis. 14(1):17–28.
Original Article