Spatiotemporal Dynamics of Phlebotomus perniciosus (Diptera: Psychodidae) and Characterization of its Habitats Using Satellite Images in Fez City, North Central Morocco http://www.doi.org/10.26538/tjnpr/v7i10.3
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Abstract
Leishmaniasis is a serious public and veterinary health concern. Species of the subgenus
Larroussius are the suspected and proven vectors of the leishmaniasis visceral form. This study
was aimed at investigating the spatiotemporal dynamics of Phlebotomus perniciosus (Diptera:
Psychodidae) and characterizing its habitats using satellite images. The entomological sampling
was based on a preliminary stratification of the study area, in which the sandflies were collected
at 12 selected stations in Fez City using sticky paper traps. The environmental factors studied for
each station were land surface temperature (LST), normalized difference vegetation index
(NDVI), and soil moisture index (SMI). Correlations between the number of species of sandflies
and each of the environmental factors were evaluated using Pearson's correlation. Differences
were considered significant at p < 0.05 (95% confidence level). Two species of the subgenus
Larroussius, which are vectors of visceral leishmaniasis, Ph. perniciosus (96.54%) and Ph.
longicuspis (3.46%), were found in the collected 231 specimens. Statistical analysis of the
environmental factors also demonstrated a significant positive correlation between the number of
Ph. perniciosus and LST in all environments. However, the correlation between the isolated
species and NDVI was not strong and only significant in the urban area (r = 0.79, p = 0.0018), and
no significant correlation was found with the SMI. The findings of this study could help health
authorities develop appropriate future vector control strategies.
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References
Benkova I, Volf P. Effect of temperature on metabolism of phlebotomus papatasi (Diptera: Psychodidae). J Med
Entomol. 2007; 44(1):150-154.
Prudhomme J, Rahola N, Toty C, Cassan C, Roiz D, Vergnes B, Thierry M, Rioux J-A, B. Alten, Sereno D, Bañuls A-L.
Ecology and spatiotemporal dynamics of sandflies in the Mediterranean Languedoc region (Roquedur area, Gard,
France). Parasites Vectors. 2015; 8(642):14. Doi: 10.1186/s13071-015-1250-2
El Omari H, Chahlaoui A, Talbi FZ, Chlouchi A, El-Akhal F, Lahouiti K, Taroq A, Alaoui M, El Ouali Lalami A. Entomological Survey and Impact of Climatic Factors on the Dynamics of Sandflies in Central Morocco. Sci World J.
; 2023:8. Doi: 10.1155/2023/6952992
World Health Organization. Weekly Epidemiological Record. Geneva. 2016; 91(22):285-296.
Gangneux J-P, Belaz S, Robert-Gangneux F. Update and news on Mediterranean visceral leishmaniasis. J Anti-Infect. 2015; 17(1):25-28.
Alkan C, Bichaud L, De Lamballerie X, Alten B, Gould EA, Charrel RN. Sandfly-borne phleboviruses of Eurasia and
Africa: Epidemiology, genetic diversity, geographic range, control measures. Antiviral Res. 2013; 100(1):54-74. Doi:
1016/j.antiviral.2013.07.005
Israël DK, Coulibaly CA, Sissoko IM, Traoré B, Wilke ABB, Beier JC, Muller GC, Doumbia S. Distribution and diversity of Sand Fly Species (Diptera: Psychodidae, Phlebotominae) in Two Geoclimatic Zones of Chad. Front Trop Dis. 2022; 2:6. Doi: 10.3389/fitd.2021.762295
Mouloua S, Boubidi SC, Bouiba L, Mezai G, Madiou M, Harrat Z. Environmental impact on the distribution of leishmaniases in the focus of Tizi-Ouzou (Algeria). Rev Med Vet. 2017; 168(10-12):252-261.
World Health Organization. Weekly Epidemiological Record. 2021; 96(35):401-420. https://www.who.int/publications/journals/weeklyepidemiological-record
Talbi FZ, Najy M, Nouayti N, En-nkhili H, El Ouali Lalami A. Cutaneous Leishmaniasis cases and risk factors in north central of Morocco, Sefrou province: An impact study. E3S Web Conf. 2021; 234(7):7. Doi: 10.1051/e3sconf/202123400027
Arroub H, Benlmekki M, Bencharki B, Bahdaoui K, Habbari K. Spatio-temporal distribution of cutaneous leishmaniasis in Moroccan semi-arid areas. IJIAS. 2016; 14:187-197.
Rhajaoui M. Human leishmaniases in Morocco: a nosogeographic diversity. Pathol Biol. 2011; 59:266-229.
Abou-Elaaz F-Z, Outourakht A, Himmi Oumnia S, Guernaoui S. Thirty years of cutaneous leishmaniasis in Tadla-Azilal focus, Morocco. Parasite Epidemiol Control. 2019; 4:e00196. Doi: 10.1016/j.parepi.2019.e00091
El-Mouhdi K, Chahlaoui A, El Ouali Lalami A, Bouzid J, El Omari H, Fekhaoui M. Epidemiological Situation of Leishmaniases at the Level of the City of El Hajeb (Central Morocco) During the Period from 2013 to 2017. Eur Sci J.
; 17(3):155-168.
Boussa S, Boumezzough A, Remy PE, Glasser N, Pesson B. Morphological and isoenzymatic differentiation of
Phlebotomus perniciosus and Phlebotomus longicuspis (Diptera: Psychodidae) in Southern Morocco. Acta Trop.
; 106(3):184–189. Doi: 10.1016/j.actatropica.2008.03.011
Belen A, Alten B. Seasonal dynamics and altitudinal distributions of sand fly (Diptera: Psychodidae) populations in a cutaneous leishmaniasis endemic area of the Cukurova region of Turkey. J Vector Ecol. 2011; 36:87-94.
Pérez J, Virgen A, JRebollar-Téllez JC, Alfredo C, Infante F, Mikery O, Marina CF, Ibànez-Bernal S. Species composition and seasonal abundance of sandflies (Diptera: Psychodidae: Phlebotominae) in coffee groecosystems. Mem Inst Oswaldo Cru. 2014; 109(1):80-86. Doi: 10.1590/0074- 0276130224
El Omari H, Chahlaoui A, Talbi FZ, Lahouiti K, Taam A, El Khayyat F, Alami A, Darkaoui N, Merabti A, Amaiach R, El
Ouali Lalami A, Leishmaniasis Risk Factors in Central Morocco: Urbanization and Socio-Economic Factors. Trop J
Nat Prod Res. 2022; 6(12):1964-1968. Doi: 10.1155/2020/2196418
Tribak A, El Amrani H, Abahrour M, Ziane FZ, Azagouagh K, En-nasry EH, Benriah N, Roudani EYS. Occupation of
high-risk sites in peri-urban areas: causes, methods and consequences: case of the cities of Fez and Taza Morocco).
Geo EcoTrop. 2019; 2(1):249-258.
Mokhtari N, Mrabet R, Lebailly P, Bock L. Spatialization of bioclimates, aridity and stages of vegetation in Morocco. Rev Mar Sci Agron Vét. 2014; 2(1):50-66.
Hakam O, Baali A, Ait Brahim Y, El Kamel T, Azennoud K. Regional and global teleconnections patterns governing rainfall in the Western Mediterranean: case of the Lower Sebou Basin, North-West Morocco. Model Earth Syst Environ. 2022; 8:5107-5128. Doi: 10.1007/s40808-022- 01425-3
High Commission for Planning of Morocco (HCP). Reportage. 2014, available on http://goo.gl/6jquVC.
El Fattouhi Y, Darkaoui N, Talbi FZ, Idrissi AJ, Lalami AEO. Knowledge, Practice, and Behavior of University Students Concerning Sandfly Vectors of Leishmaniasis in Fez City, Central North Morocco. Trop J Nat Prod Res. 2023; 7(6):2837-2844.
Talbi FZ, Merabti A, El-Akhal F, Alami A, El Omari H, Najy M, Amaiach R, Mrani Alaoui M, Taroq A, El Khayyat F,
Benboubker M, Hilali S, El Ouali Lalami A. Influence of Basic Environmental Factors on Seasonal Variation and
Distribution of Sand Flies at Ben Slimane Sites in Fez City, Morocco. Trop J Nat Prod Res. 2022; 6(9):1391-1395.
Buchhorn M, Smets B, Bertels L, De Roo B, Lesiv M, Tsendbazar NE, Herold M, Fritz S. Copernicus Global Land Service: Land Cover 100m: collection 3: epoch 2018: Globe. Zenodo. 2020; Doi: 10.5281/zenodo.3518038
Talbi FZ, Idrissi Janati A, Fadil M, El Omari H, El-Akhal F, Mrani Alaoui M, Nouayti N, Alami A, Taam A, Hilali S,
Amaiach R, Taroq A, El-Khayyat F, Merabti A, El Ouali Lalami A. Distribution and Abundance of Sand Flies in Five
Selected Communities in Communities in Fez, Morocco, and Impact of Climatic Factors. Trop J Nat Prod Res. 2022;
(9):1405-1410.
Abonnenc E. The sandflies of the Ethiopian region (Diptera: Phlebotomidae). Memoir of Orstom. 1972; 55:289.
Pesson B, Ready JS, Benabdennbi I, Martin-Sanchez J, Esseghir S, Cadi-Soussi M, Morillas-Marquez F, Ready PD.
Sandflies of the Phlebotomus perniciosus complex: mitochondrial introgression and a new sibling species of P.
longicuspis in the Moroccan Rif. Med Vet Entomol. 2004; 18(1):25-37. Doi: 10.1111/j.0269-283x.2004.0471.x
Faraj C, Himmi O. Clés morphologiques pour l'identification des phlébotomes du Maroc (Diptera : Psychodidae : Phlebotominae). Bull Soc Pathol Exot. 2020; 113:155-174. Doi : 10.3166/bspe-2020-0137
Ministry of Health. Fight against Leishmaniasis, Activity Guide, Ministry of Health, Rabat, Morocco, 2010.
Berchi S, Bounamous A, Louadi K, Pesson B. Morphological distinction between two sympatric species: Phlebotomus perniciosus and Phlebotomus longicuspis (Diptera: Psychodidae). Ann Soc Entomol Fr. 2007; 43(2):201–203.
Benallal KE, Benikhlef B, Garni R, Gassen B, Débet JP, Harra Z. Presence of Phlebotomus perniciosus Atypical
Form in Algeria. J Arthropod-Borne Dis. 2017; 11(1):139- 146.
Faraj C, Himmi O. Liste actualisée des Phlebotominae (Diptera : Psychodidae) du Maroc. Bull Soc Pathol Exot.
; 112:296–301 Doi: 10.3166/bspe-2020-0107
Hakam O, Baali A, Azennoud K, Lyazidi A, Bourchachen M. Assessments of Drought Effects on Plant Production
Using Satellite Remote Sensing Technology, GIS and Observed Climate Data in Northwest Morocco, Case of the Lower Sebou Basin. Int J Plant Prod. 2023; 17(4): Doi: 10.1007/s42106-023-00236-5
Landsat. Project Science Office, Landsat 7 Science Data User's Handbook. Goddard Space Flight Center, Greenbelt, MD, 2002.
Dash P, Göttsche FM, Olesen FS, Fischer H. Land surface temperature and emissivity estimation from passive senor data: Theory and practice-current trends. Int J Remote Sens 2002; 23(13):2563-2594. Doi: 10.1080/01431160110115041
Snyder WC, Wan Z, Zhang Y, Feng YZ. Classification-based emissivity for land surface temperature measurement from space. Int J Remote Sens. 1998; 19(14):2753–2774.
Artis DA, Carnahan WH. Survey of emissivity variability in thermography of urban areas. Remote Sens Environ. 1982; 12(4):313-329.
Moawad BM. Geoscience general tool package. Max-Planck Institute für Chemie, Mainz, Germany. 2012.
Daoudi M, Boussaa S, Hafidi M, Boumezzough A. Potential distributions of phlebotomine sandy vectors of human visceral leishmaniasis caused by Leishmania infantum in Morocco. Med Vet Entomol. 2020; 34(4):385-393. Doi: 10.1111/mve.12434
Ouanaimi F, Boussaa S, Boumezzough A. Phlebotomine sand flies (Diptera: Psychodidae) of Morocco: results of an entomological survey along three transects from northern to southern country. Asian Pac J Trop Dis. 2015; 5(4):299-306. Doi: 10.1016/S2222-1808(14)60787-8
Talbi FZ, Aarab L, Faraj C, Idrissi AJ, El Ouali Lalami A. Monitoring of vector-borne Diseases: Investigation of Feeding Preferences of the Sand Fly, Phlebotomus perniciosus (Diptera: Psychodidae) in a focus of cutaneous
leishmaniasis in Aichoun, North center of Morocco. Int J Pharm Sci Rev Res. 2016; 41(11):48-52.
Ramdane E, Berchi S, Louadi K. Sandflies (Diptera, Pshycodidae), vectors of pathogens responsible for human
leishmaniasis in the region of Constantine (Algeria). Entomofauna. 2018; 32(2):537-555.
Berdjane-Brouk Z, Charrel RN, Hamrioui B, Izri A. First detection of Lieshmania infantum DNA in Phlebotomus
longicuspis Nitzulescu, 1930 from visceral leishmaniasis endemic focus in Algeria. Parasitol Res. 2012; 111(1):419-
Doi: 10.1007/s00436-012-2858-1
Dedet JP. Leishmaniases in Metropolitan France. BEH Special Edition. 2010. 9-12.
Bailly-Choumara H, Abonnenc E, Pastre J. Contribution to the study of sandflies in Morocco (Diptera, Psychodidae) Faunistic and ecological data. Ent Méd Parasitol. 1971; 4:431-460.
Ballart C, Barón S, Alcover MM, Portús M, Gállego M. Distribution of phlebotomine sand flies (Diptera:
Psychodidae) in Androrra: First finding of P. perniciosus and wide distribution of P. ariasi. Acta Trop. 2012; 22(1):155- 159. Doi: 10.1016/j.actatropica.2011.11.011
Rioux JA, Rispail P, Lanotte G, Lepart J. Relationship between sandflies and bioclimates in leishmaniasis ecology.
Epidemiological corollaries. The example of Morocco. Taureau Soc Bot Pr. 1984; 131:549–557.
Guernaoui S, Boumezzough A. Habitat Preferences of Phlebotomine Sand Flies (Diptera: Psychodidae) in
Southwestern Morocco. J. Med. Entomol. 2009; 45(5):1187- 1194.
El Omari H, Chahlaoui A, Ouarrak K, El Ouali Lalami A. Surveillance of leishmaniases: inventory and seasonal fluctuation of sandflies (Diptera: psychodidae) in the prefecture of Meknes (central Morocco). Bull Soc Pathol
Exot. 2018; 111(5):309–315. Doi: 10.3166/bspe-2019-0 61
Talbi FZ, Faraj C, El-Akhal F, El Khayyat F, Chenfour D, Janati Idrissi A, El Ouali Lalami A. Diversity and Dynamics
of Sand Flies (Diptera: Psychodidae) of Two Cutaneous Leishmaniasis Foci in the Fes-Boulemane Region of
Northern Morocco. Int J Zool. 2015; 2015(4-5):1-6. Doi: 10.1155/2015/497169
Lahouiti K, El Ouali Lalami A, Maniar S, Bekhti K. Seasonal fluctuations of phlébotomines sand fly populations (Diptera: Psychodidae) in the Moulay Yacoub province, centre Morocco: Effect of ecological factors. Afr J Environ Sci
Technol. 2013; 7(11):1028-1036. Doi:10.5897/AJEST2013.1549
Darkaoui N, Janati Idrissi A, Talbi FZ, El Fattouhi Y, Taam A, Nouayti N, El Ouali Lalami A. Taxonomic study of the
phlebotomian biodiversity of Fez city (Central Morocco). Tropical Journal of Natural Product Research. 2022; 6(5)894-899. Doi: 10.26538/tjnpr/v6i6.12
Faraj K, Bekhti K, Fadil M et al. Entomological investigations in moulay Yaacoub, leishmaniasis focus in the
center of Morocco. Asian J Pharm Clin Res. 2016; 9:340–345.
Muñoz C, Risueño J, Pérez-Cutillas P, Bernal LJ, Ortiz JM,Ruiz de Ybáñez R, Sánchez-López PF, Martinez-Carrasco ,
Del Río L, De la Rúa P, García-Martínez JD, Gonzálvez M, Murcia L, Collantes F, Goyena E, Spitzova T, Elshanat S,
Berriatua E. Density assessment and reporting for Phlebotomus perniciosus and other sand fly species in periurban residential estates in Spain. Parasitol Res. 2021; 120(9):3091-3103. Doi: 10.1007/s00436-021-07270-0
Abdullah AYM, Dewan A, Shogib MRI, Rahman MM, Hossain MF. Environmental factors associated with thedistribution of visceral leishmaniasis in endemic areas of Bangladesh: modeling the ecological niche. Trop Med
Health. 2017; 45(13):1-15. Doi: 10.1186/s41182-017-0054-9
Kone K, Diarra AZ, Coulibaly M, Niaré S, Berthe M, TraoréA, Ongoiba A, Dado A, Thera MA, Izri A, Doumbo OK.
Spatio-temporal distribution of the sandfly fauna in urban and peri-urban areas of Bamako, Mali. Ann Soc Entomol Fr. 2016; 52:95-101. Doi: 10.1080/00379271.2016.1194773
Colacicco-Mayhugh MG, Masuoka PM, Grieco JP. Ecological niche model of Phlebotomus alexandri and P.
papatasi (Diptera: Psychodidae) in the Middle East. Int J Health Geogr. 2010; 9(1):2. Doi:10.1186/1476-072X-9-2
Talbi FZ, Najy M, Fadil M, Nouayti N, El Ouali Lalami A.Diversity and Seasonal Occurrence of Sand Flies and the Impact of Climatic Change in Aichoune Locality, Central Morocco. Innovations in Smart Cities Applications Volume
2020; 183:583-593. Doi: 10.1007/978-3-030-66840-2_44
El Omari H, Chahlaoui A, Talbi FZ, El Mouhdi K, EL Ouali Lalami A. Impact of Climatic on the Seasonal Fluctuation of Leishmaniasis Vectors in Central Morocco (Meknes Prefecture). Can J Infect Dis Med Microbiol. 2020; 2020:1-
Doi: 10.1155/2020/6098149
Kesari S, Bhunia GS, Chatterjee N, Kumar V, Mandal R, Das P. Assessment of habitat suitability of Phlebotomus
argentipes using a remote sensing index in the Kala-azar endemic focus of Bihar, India. Men Inst Oswaldo Cruz. 2018; 108:197-204.
Bounoua L, Houti K, Blakey T, Ebi KL, Zhang P, Imhoff ML, Thome KJ, Dudek C, Sahabi SA, Messouli M,
Makhlouf B, El Laamrani A, Boumezzough A. Linking climate to incidence of zoonotic cutaneous leishmaniasis (L.
major) in pre-saharan North Africa. Int J Environ Res Public Health. 2013; 10(8):3172-3191. Doi: 10.3390/ijerph10083172
Boussaa S, Kahime K, Samy AM, Salem AB, Boumezzough A. Species composition of sand flies and bionomics of
Phlebotomus papatasi and P. sergenti (Dipera: Psychodidae) in cutaneous leishmaniaisis endemic foci, Morocco. Parasites Vectors. 2016; 9(60).
Rodgers MSM, Bavia ME, Fonseca EOL, Cova BO, Silva MMN, Carneiro DDMT, Cardim LL, Malone JB. Ecological
niche models for sand fly species and predicted distribution of Lutzomyia longipalpis (Diptera: Psychodidae) and
visceral leishmaniasis in Bahia state, Brazil. Environ Monit Assess. 2019; 191(2):331. Doi: 10.1007/s10661-019-7431-2
Signorini M, Cassini R, Drigo M, Di Regalbono AF, Pietrobelli M, Montarsi F, Stensgaard AS. Ecological niche
model of Phlebotomus perniciosus, the main vector of canine in north-eastern Italy. Geospat Health. 2014; 9(1):193-201. Doi: 10.4081/gh.2014.16
Gebre-Michael T, Malone J, Balkew M, Ali A, Berhe N, Hailu A, Herzi AA. Mapping the potential distribution of
Phlebotomus martini and P. orientalis (Diptera: Psychodidae), vectors of kala-azar in East Africa by use of geographic information systems. Acta Trop. 2004; 90(1):73–86. Doi: 10.1016/j.actatropica.2003.09.021
Li W, Cao Q, Lang K, Wu J. Linking potential heat sourceand sink to urban heat island: heterogeneous effects of
landscape pettern on land surface temperature. Sci Total Environ. 2017; 586:457-465. Doi: 10.1016/j.scitotenv.2017.01.191
Barón SD, Morillas-Márquez F, Morales-Yuste M, DíazSáez V, C. Irigaray C, Martín-Sánchez J. Risk maps for the presence and absence of Phlebotomus perniciosus in an endemic area of leishmaniasis in southern Spain:
implications for the control of the disease. Parasitology. 2011; 138(10):1234-1244.Doi: 10.1017/S0031182011000953