Parasitology Research

, Volume 117, Issue 4, pp 1105–1113 | Cite as

Phlebotomus langeroni Nitzulescu (Diptera, Psychodidae) a new vector for Leishmania infantum in Europe

  • Victoriano Díaz Sáez
  • F. Morillas-Márquez
  • G. Merino-Espinosa
  • V. Corpas-López
  • M. Morales-Yuste
  • B. Pesson
  • S. Barón-López
  • J. Lucientes-Curdi
  • J. Martín-Sánchez
Original Paper


Burrows of the wild rabbit, Oryctolagus cuniculus, a lagomorph that has been recently suggested as a Leishmania infantum reservoir, constitute an unspoilt biotope in phlebotomine studies in Europe. We hypothesize that Phlebotomus langeroni, a proven vector of L. infantum in North Africa, is associated with rabbits and may have been overlooked in Europe. Sandfly captures were carried out with CDC light traps in an L. infantum endemic area of southern Spain with a high density of lagomorphs and a large numbers of burrows. The stable, permanent, and highly abundant presence of P. langeroni was assessed. After morphological identification, this sandfly species was characterized by comparing it with P. perniciosus and other P. langeroni populations from North Africa through molecular techniques. P. langeroni had not been found in southern Spain to date, despite being a highly investigated area, except for this particular biotope. Its activity period turned out to begin in mid-July, ending in late October, accounting for a maximum activity during this month. This study shows that P. langeroni is associated with the existence of rabbit burrows and has been overlooked in Europe. L. infantum DNA was found in almost half of the female specimens (47.6%) captured inside a biotope where wild rabbits are infected as well.


Phlebotomus langeroni Leishmania infantum Europe Wild rabbit burrows Oryctolagus cuniculus 


Funding information

The authors wish to thank the Spanish Ministry of Science and Innovation for funding this research through the Project CGL2007-66943-C02-02/BOS and the Junta de Andalucía for the project P07-CVI-03249, and the research group CVI176. Thanks also to the staff of administration and services of the state “La Torre” (Illora) for their strong support and generous collaboration for the execution of the present work.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Alcover MM, Gramiccia M, Di Muccio T, Ballart C, Castillejo S, Picado A, Portús M, Gállego M (2012) Application of molecular techniques in the study of natural infection of Leishmania infantum vectors and utility of sandfly blood meal digestion for epidemiological surveys of leishmaniasis. Parasitol Res 111(2):515–523. CrossRefPubMedGoogle Scholar
  2. Alten B, Maia C, Odete M, Campino L, Jiménez M, González E, Molina R, Bañuls A L, Prudhomme J, Vergnes B, Toty C, Cassan C, Rahola N, Thierry M, Sereno D, Bongiorno G, Bianchi R, Khoury C, Tsirigotakis N, Dokianakis E, Antoniou M, Christodoulou V, Mazeris A, Karakus M, Ozbel Y, Arserim S K, Kasap O E, Gunay F, Oguz G, Kaynas S, Tsertsvadze N, Tskhvaradze L, Giorgobiani E, Gramiccia M, Volf P, Gradoni L (2016) Seasonal dynamics of phlebotomine sand fly species proven vectors of Mediterranean leishmaniasis caused by Leishmania infantum. PLoS Negl Trop Dis 1-22. DOI:
  3. Antoniou M, Gramiccia M, Molina R, Dvorak V, Volf P (2013) The role of indigenous phlebotomine sandflies and mammals in the spreading of leishmaniasis agents in the Mediterranean region. Euro Surveill 18(30):20540CrossRefPubMedGoogle Scholar
  4. Ballart C, Guerrero I, Castells X, Barón S, Castillejo S, Alcover MM, Portús M, Gállego M (2014) Importance of individual analysis of environmental and climatic factors affecting the density of Leishmania vectors living in the same geographical area: the example of Phlebotomus ariasi and P. perniciosus in northeast Spain. Geospat Health 8(2):389–403. CrossRefPubMedGoogle Scholar
  5. Barhoumi W, Qualls WA, Archer RS, Fuller DO, Chelbi I, Cherni S, Derbali M, Arheart KL, Zhioua E, Beier JC (2015) Irrigation in the arid regions of Tunisia impacts the abundance and apparent density of sand fly vectors of Leishmania infantum. Acta Trop 141(Pt A):73–78. CrossRefPubMedGoogle Scholar
  6. Barón S, Martín-Sánchez J, Gállego M, Morales-Yuste M, Boussaa S, Morillas-Márquez F (2008) Intraspecific variability (rDNA ITS and mtDNA Cyt b) of Phlebotomus sergenti in Spain and Morocco. Acta Trop 107(3):259–267. CrossRefPubMedGoogle Scholar
  7. Barón SD, Morillas-Márquez F, Morales-Yuste M, Díaz-Sáez V, Irigaray C, Martín-Sánchez J (2011) 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 138(10):1234–1244. CrossRefPubMedGoogle Scholar
  8. Croset H, Rioux JA, Maistre M, Bayar N (1978) Les Phlébotomes de Tunisie (Diptera-Phlebotominae). A revision of the systematics, distribution and behaviour. Ann Parasitol Hum Comp 53:711–749CrossRefPubMedGoogle Scholar
  9. Díaz-Sáez V, Merino-Espinosa G, Morales-Yuste M, Corpas-López V, Pratlong F, Morillas-Márquez F, Martín-Sánchez J (2014) High rates of Leishmania infantum and Trypanosoma nabiasi infection in wild rabbits (Oryctolagus cuniculus) in sympatric and syntrophic conditions in an endemic canine leishmaniasis area: epidemiological consequences. Vet Parasitol 202(3–4):119–127. CrossRefPubMedGoogle Scholar
  10. Doha S, Shehata MG (1992) Leishmania infantum MON-98 isolated from naturally infected Phlebotomus langeroni Nitzulescu in El Hammam Mathroug Egypt. Ann Parasitol Hum Comp 2:69–76Google Scholar
  11. El Sawaf B, Kassem HA, El Said S (1985) Description of the unknown female of Phlebotomus langeroni (Diptera, Psychodidae). J Med Ent 22(3):312–314. CrossRefGoogle Scholar
  12. El Sawaf BM, Mansour NS, El Said SM, Daba S, Youssef FG, Kenawy MA, Beier JC (1989) Feeding patterns of Phlebotomus papatasi and Phlebotomus langeroni (Diptera: Psychodidae) in El Agamy, Egypt. J Med Entomol 26(5):497–498. CrossRefPubMedGoogle Scholar
  13. Esseghir S, Ready PD, Killick-kendrick R, Ben-Isamil R (1997) Mitochondrial haplotypes and phylogeography of Phlebotomus vectors of Leishmania major. Insect Mol Biol 6(3):211–225. CrossRefPubMedGoogle Scholar
  14. Esseguir S, Ready PD (2000) Speciation of Phlebotomus sandflies of the subgenus Larroussius coincided with the late Miocene-Pliocene aridification of the Mediterranean subregion. Biol J Linn Soc Lond 70(2):189–219. CrossRefGoogle Scholar
  15. Es-Sette N, Ajaoud M, Laamrani-Idrissi A, Mellouki F, Lemrani M (2014) Molecular detection and identification of Leishmania infection in naturally infected sand flies in a focus of cutaneous leishmaniasis in northern Morocco. Parasit Vectors 7:305. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Fares W, Charrel RN, Dachraoui K, Bichaud L, Barhoumi W, Derbali M, Cherni S, Chelbi I, de Lamballerie X, Zhiouaa E (2015) Infection of sand flies collected from different bio-geographical areas of Tunisia with phleboviruses. Acta Trop 141(Pt A):1–6. CrossRefPubMedGoogle Scholar
  17. Franco ALF, Morillas-Márquez F, Barón SD, Morales-Yuste M, Gálvez R, Díaz V, Pesson B, Alves-Pires C, Depaquit J, Molina R, Afonso MO, Gállego M, Guernaoui S, Bounamous A, Martín-Sánchez J (2010) Genetic structure of Phlebotomus (Larroussius) ariasi populations, the vector of Leishmania infantum in the western Mediterranean: epidemiological implications. Intern J Parasitol 40:1335–1346CrossRefGoogle Scholar
  18. Gálvez R, Descalzo MA, Guerrero I, Miró G, Molina R (2011) Mapping the current distribution and predicted spread of the leishmaniosis sand fly vector in the Madrid region (Spain) based on environmental variables and expected climate change. Vector Borne Zoonotic Dis 11(7):799–806. CrossRefPubMedGoogle Scholar
  19. Ghrab J, Rhim A, Hamba DB, Aoun K, Bouratbine A (2005) Phlebotomus (Larroussius) langeroni Nitzulescu, 1930 in Tunisia: presence of the female and updating of geographical distribution. Bull Soc Pathol Exot 98(5):411–412PubMedGoogle Scholar
  20. Gil Collado J, Morillas Márquez F, Sanchís Marín MC (1989) Los flebotomos en España. Rev Sanid Hig Publica 63:15–34PubMedGoogle Scholar
  21. Giorgobiani E, Lawyer PG, Babuadze G, Dolidze N, Jochim RC, Tskhvaradze L, Kikaleishvili K, Kamhawi S (2012) Incrimination of Phlebotomus kandelakii and Phlebotomus balcanicus as vectors of Leishmania infantum in Tbilisi, Georgia. PLoS Negl Trop Dis 6(4):e1609. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Guerbouj S, Chemkhi J, B K, A R, Ben Ismail R, Guizani I (2007) Natural infection of Phlebotomus (Larroussius) langeroni (Diptera: Psychodidae) with Leishmania infantum in Tunisia. Trans R Soc Trop Med Hyg 101(4):372–377CrossRefPubMedGoogle Scholar
  23. Haddad N, Léger N, Sadek R (2003) Sandflies of Lebanon: faunistic inventory. Parasite 10(2):99–110CrossRefPubMedGoogle Scholar
  24. Jiménez M, González E, Martín-Martín I, Hernández S, Molina R (2014) Could wild rabbits (Oryctolagus cuniculus) be reservoirs for Leishmania infantum in the focus of Madrid, Spain? Vet Parasitol 202(3–4):296–300. CrossRefPubMedGoogle Scholar
  25. Kassem HA, El Nogoumy NN, El Sawaf BM (2012) Impact of urbanization on the sand fly Phlebotomus langeroni Nitzulescu in an old focus of visceral leishmaniasis in Egyp. J Egypt Soc Parasitol 42(3):619–624CrossRefPubMedGoogle Scholar
  26. Killick-Kendrick R (1990) Phlebotomine vectors of the leishmaniases: a review. Med Vet Entomol 4(1):1–24. CrossRefPubMedGoogle Scholar
  27. Leger N, Pesson B, Madulo-Leblond G, Abonnenc E (1983) Sur la differentiation des femelles du sous-genre Larroussius Nitzulescu, 1931. (Diptera, Phlebotomidae) de la región mediterranéenne. Ann Parasitol Hum Comp 58(6):611–623. CrossRefPubMedGoogle Scholar
  28. Lucientes J, Osacar JJ, Caliente C, Benito I, Castillo JA (1994) Sobre la presencia de Phlebotomus (Larroussius) langeroni Nitzulescu, 1930 (Diptera: Psychodidae) en Aragón. ZAPATERI Revta Aragon Ent 4:19–22Google Scholar
  29. Martínez Ortega E, Conesa Gállego E, Goyena Salgado M, Romera Lozano H (1992) Presencia de Phlebotomus (Larroussius) langeroni Nitzulescu, 1930 (Diptera: Psychodidae) en la Península Ibérica. Bolm Soc Port Ent 139(7):196Google Scholar
  30. Martínez Ortega E, Conesa Gállego E, Romera Lozano H (1996) Phlebotomus (Larroussius) langeroni Nitzulescu, 1930 (Diptera: Psychodidae), espèce nouvelle pour l’Espagne. Parasite 3:77–80CrossRefGoogle Scholar
  31. Martín-Sánchez J, Gállego M, Barón S, Castillejo S, Morillas-Márquez F (2006) Pool screen PCR for estimating the prevalence of Leishmania infantum infection in sandflies (Diptera: Nematocera, Phlebotomidae). Trans R Soc Trop Med Hyg 100:527–532CrossRefPubMedGoogle Scholar
  32. Martín-Sánchez J, Gramiccia M, Di Muccio T, Ludovisi A, Morillas-Márquez F (2004) Isoenzymatic polymorphism of Leishmania infantum in southern Spain. Trans R Soc Trop Med Hyg 98(4):228–232CrossRefPubMedGoogle Scholar
  33. Martín-Sánchez J, Guilvard E, Acedo-Sánchez C, Wolf-Echeverri M, Sanchís-Marín MC, Morillas-Márquez F (1994) Phlebotomus perniciosus Newstead, 1911, infection by various zymodemes of the Leishmania infantum complex in the Granada province (southern Spain). Int J Parasitol 24(3):405–408. CrossRefPubMedGoogle Scholar
  34. Martín-Sánchez J, López-López MC, Acedo-Sánchez C, Castro-Fajardo JJ, Pineda JA, Morillas-Márquez F (2001) Diagnosis of infections with Leishmania infantum using PCR-ELISA. Parasitology 122(Pt 6):607–615PubMedGoogle Scholar
  35. Martín-Sánchez J, Morales-Yuste M, Acedo-Sánchez C, Barón S, Díaz V, Morillas-Márquez F (2009) Canine leishmaniasis in southeastern Spain. Emerg Infect Dis 15(5):795–798. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Molina R, Jiménez MI, Cruz I, Iriso A, Martín-Martín I, Sevillano O, Melero S, Bernal J (2012) The hare (Lepus granatensis) as potential sylvatic reservoir of Leishmania infantum in Spain. Vet Parasitol 190(1–2):268–271. CrossRefPubMedGoogle Scholar
  37. Morales-Yuste M, Morillas-Márquez F, Díaz-Sáez V, Barón-López S, Acedo-Sánchez C, Martín-Sánchez J (2012) Epidemiological implications of the use of various methods for the diagnosis of canine leishmaniasis in dogs with different characteristics and in differing prevalence scenarios. Parasitol Res 111 (1): 155–164. doi:, 1
  38. Morillas F, Sánchez Rabasco F, Ocaña J, Martín-Sánchez J, Ocaña-Wihelmi J, Acedo C, Sanchís-Marin MC (1996) Leishmaniosis in the focus of the Axarquía region, Malaga province, southern Spain: a survey of the human, dog, and vector. Parasitol Res 82(6):569–570CrossRefPubMedGoogle Scholar
  39. Morillas-Márquez F, Guevara Benítez DC, Úbeda Ontiveros JM, González Castro J (1983) Fluctuations annuelles des populations de phlébotomes (Diptera, Phlebotomidae) dans la province de Grenade (Espagne). Ann Parasitol Hum Comp 58(6):625–632. CrossRefPubMedGoogle Scholar
  40. Morillas-Márquez F, Martín-Sánchez J, Díaz-Sáez V, Barón-López S, Morales-Yuste M, Alves de Lima Franco F, Sanchís-Marín MC (2010) Climate change and infectious diseases in Europe: leishmaniosis and its vectors in Spain. Lancet Infect Dis 10:216–217CrossRefPubMedGoogle Scholar
  41. Navea-Pérez HM, Díaz-Sáez V, Corpas-López V, Merino-Espinosa G, Morillas-Márquez F, Martín-Sánchez J (2015) Leishmania infantum in wild rodents: reservoirs or just irrelevant incidental hosts? Parasitol Res 113:2363–2370CrossRefGoogle Scholar
  42. Nitzulescu V (1930) Phlebotomus langeroni n. sp. et Phlebotomus langeroni var. longicuspis n var. de Douart-shott (Tunisie). Ann Parasitol Hum Comp 8(5):547–553. CrossRefGoogle Scholar
  43. Ouanaimi F, Boussaa S, Boumezzough A (2015) Phlebotomine sandflies (Diptera, Psychodidae) of Morocco: results of an entomological survey along three transects from northern to southern country. Asian Pac J Trop Dis 5:299–306CrossRefGoogle Scholar
  44. Ready PD (2010) Leishmaniasis emergence in Europe. Euro Surveill 15(10):19505PubMedGoogle Scholar
  45. Rioux JA, Carron S, Dereure J, Périères J, Zeraia L, Franquet E, Babinot M, Gállego M, Prudhomme J (2013) Ecology of leishmaniasis in the South of France, 22. Reliability and representativeness of 12 Phlebotomus ariasi, P. perniciosus and Sergentomyia minuta (Diptera: Psychodidae) sampling stations in Vallespir (eastern French Pyrenees region). Parasite 20:34CrossRefPubMedPubMedCentralGoogle Scholar
  46. Rioux JA, Lanotte G, Petter F, Dreure J, Akalay O, Pratlong F, Velez ID, Fikri NB, Maazoun R, Denial M, Jarry DM, Zahaf A, Ashford RW, Cadi-Soussi M, Killick-Kendrick R, Benmansour N, Moreno G, Périères J, Guilvard E, Zribi M, Kennou MF, Rispail P, Knechtli R, Serres E (1986) jht Les leishmanioses cutanées du bassin Méditerranéen occidental. De l’identification enzymatique à l’analyse éco-épidemiologique. L’example du trois foyers, tunisien, marocain, et français. In : Leishmania. Taxonomie et phylogenese. Applications éco-épidémiologiques. Montpellier, pp 365–395Google Scholar
  47. Rivas Martínez S, Gandullo JM, Serrada R, Allué Andrade JL, Montero de Burgos JL, González Rebollar JL (1987) Memoria del mapa de series de vegetación de España. Ministerio de Agricultura, Pesca y Alimentación, ICONA, Madrid, pp 31–42Google Scholar
  48. Schuh C (1999) Phlebotomus (Larroussius) langeroni (Diptera, Psychodidae) : données morphologiques et isoenzymatiques. Mem. Diplôme d’etat de docteur en Pharmacie, Université L. Pasteur Strasbourg, FranceGoogle Scholar
  49. Wagué M, Aziz A, Depaquit J, Ferté H, Ndao M, Elguero E, Gaye O, Alten B, Perktas U, Cassan C, Faye B, Bañuls AL (2016) Transmission of Leishmania infantum in the canine Leishmaniasis focus of Mont-Rolland, Senegal: ecological, parasitological and molecular evidence for a possible role of Sergentomyia sand flies. PLoS Negl Trop Dis 10(11):e0004940. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Victoriano Díaz Sáez
    • 1
    • 2
  • F. Morillas-Márquez
    • 1
  • G. Merino-Espinosa
    • 1
  • V. Corpas-López
    • 1
  • M. Morales-Yuste
    • 1
  • B. Pesson
    • 2
  • S. Barón-López
    • 1
  • J. Lucientes-Curdi
    • 3
  • J. Martín-Sánchez
    • 1
  1. 1.Departament of Parasitology, Faculty of PharmacyUniversity of GranadaGranadaSpain
  2. 2.Laboratory of ParasitologyUniversity of StrasbourgStrasbourgFrance
  3. 3.Department of Animal Pathology, Faculty of VeterinaryUniversity of ZaragozaZaragozaSpain

Personalised recommendations