title: Seasonal Dynamics of Phlebotomine Sand Fly Species Proven Vectors of Mediterranean Leishmaniasis Caused by Leishmania infantum.
abstract: BACKGROUND
  The recent geographical expansion of phlebotomine vectors of Leishmania infantum in the Mediterranean subregion has been attributed to ongoing climate changes. At these latitudes, the activity of sand flies is typically seasonal; because seasonal phenomena are also sensitive to general variations in climate, current phenological data sets can provide a baseline for continuing investigations on sand fly population dynamics that may impact on future scenarios of leishmaniasis transmission. With this aim, in 2011-2013 a consortium of partners from eight Mediterranean countries carried out entomological investigations in sites where L. infantum transmission was recently reported.
  
  
  RESULTS
  A common protocol for sand fly collection included monthly captures by CDC light traps, complemented by sticky traps in most of the sites. Collections were replicated for more than one season in order to reduce the effects of local weather events. In each site, the trapping effort was left unchanged throughout the survey to legitimate inter-seasonal comparisons. Data from 99,000 collected specimens were analyzed, resulting in the description of seasonal dynamics of 56,000 sand flies belonging to L. infantum vector species throughout a wide geographical area, namely P. perniciosus (Portugal, Spain and Italy), P. ariasi (France), P. neglectus (Greece), P. tobbi (Cyprus and Turkey), P. balcanicus and P. kandelakii (Georgia). Time of sand fly appearance/disappearance in collections differed between sites, and seasonal densities showed variations in each site. Significant correlations were found between latitude/mean annual temperature of sites and i) the first month of sand fly appearance, that ranged from early April to the first half of June; ii) the type of density trend, varying from a single peak in July/August to multiple peaks increasing in magnitude from May through September. A 3-modal trend, recorded for P. tobbi in Cyprus, represents a novel finding for a L. infantum vector. Adults ended the activity starting from mid September through November, without significant correlation with latitude/mean annual temperature of sites. The period of potential exposure to L.infantum in the Mediterranean subregion, as inferred by adult densities calculated from 3 years, 37 sites and 6 competent vector species, was associated to a regular bell-shaped density curve having a wide peak center encompassing the July-September period, and falling between early May to late October for more than 99% of values. Apparently no risk for leishmaniasis transmission took place from December through March in the years considered. We found a common pattern of nocturnal females activity, whose density peaked between 11 pm and 2 am.
  
  
  CONCLUSIONS
  Despite annual variations, multiple collections performed over consecutive years provided homogeneous patterns of the potential behavior of leishmaniasis vectors in selected sites, which we propose may represent sentinel areas for future monitoring. In the investigated years, higher potential risk for L. infantum transmission in the Mediterranean was identified in the June-October period (97% relative vector density), however such risk was not equally distributed throughout the region, since density waves of adults occurred earlier and were more frequent in southern territories.
authors.affiliation: Department of Biology, Ecology Division, HUESRL-VERG laboratories, Hacettepe University, Ankara, Turkey.
authors.forename: Bulent
authors.initials: B
authors.lastname: Alten
authors.affiliation: Instituto de Higiene e Medicina Tropical, Unidade Parasitologia Médica, Universidade Nova de Lisboa, Portugal.
authors.forename: Carla
authors.initials: C
authors.lastname: Maia
authors.affiliation: Instituto de Higiene e Medicina Tropical, Unidade Parasitologia Médica, Universidade Nova de Lisboa, Portugal.
authors.forename: Maria Odete
authors.initials: MO
authors.lastname: Afonso
authors.affiliation: Instituto de Higiene e Medicina Tropical, Unidade Parasitologia Médica, Universidade Nova de Lisboa, Portugal.
authors.forename: Lenea
authors.initials: L
authors.lastname: Campino
authors.affiliation: Centro Nacional de Microbiologia, Servicio de Parasitología, Unidad de Entomología Médica, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain.
authors.forename: Maribel
authors.initials: M
authors.lastname: Jiménez
authors.affiliation: Centro Nacional de Microbiologia, Servicio de Parasitología, Unidad de Entomología Médica, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain.
authors.forename: Estela
authors.initials: E
authors.lastname: González
authors.affiliation: Centro Nacional de Microbiologia, Servicio de Parasitología, Unidad de Entomología Médica, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain.
authors.forename: Ricardo
authors.initials: R
authors.lastname: Molina
authors.affiliation: Institut de Recherche pour le Développement, MIVEGEC, Montpellier, France.
authors.forename: Anne Laure
authors.initials: AL
authors.lastname: Bañuls
authors.affiliation: Institut de Recherche pour le Développement, MIVEGEC, Montpellier, France.
authors.forename: Jorian
authors.initials: J
authors.lastname: Prudhomme
authors.affiliation: Institut de Recherche pour le Développement, MIVEGEC, Montpellier, France.
authors.forename: Baptiste
authors.initials: B
authors.lastname: Vergnes
authors.affiliation: Institut de Recherche pour le Développement, MIVEGEC, Montpellier, France.
authors.forename: Celine
authors.initials: C
authors.lastname: Toty
authors.affiliation: Institut de Recherche pour le Développement, MIVEGEC, Montpellier, France.
authors.forename: Cécile
authors.initials: C
authors.lastname: Cassan
authors.affiliation: Institut de Recherche pour le Développement, MIVEGEC, Montpellier, France.
authors.forename: Nil
authors.initials: N
authors.lastname: Rahola
authors.affiliation: Institut de Recherche pour le Développement, MIVEGEC, Montpellier, France.
authors.forename: Magali
authors.initials: M
authors.lastname: Thierry
authors.affiliation: Institut de Recherche pour le Développement, MIVEGEC, Montpellier, France.
authors.forename: Denis
authors.initials: D
authors.lastname: Sereno
authors.affiliation: M.I.P.I. Department, Unit of Vector-borne Diseases and International Health, Istituto Superiore di Sanità, Rome, Italy.
authors.forename: Gioia
authors.initials: G
authors.lastname: Bongiorno
authors.affiliation: M.I.P.I. Department, Unit of Vector-borne Diseases and International Health, Istituto Superiore di Sanità, Rome, Italy.
authors.forename: Riccardo
authors.initials: R
authors.lastname: Bianchi
authors.affiliation: M.I.P.I. Department, Unit of Vector-borne Diseases and International Health, Istituto Superiore di Sanità, Rome, Italy.
authors.forename: Cristina
authors.initials: C
authors.lastname: Khoury
authors.affiliation: Laboratory of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine, University of Crete, Heraklion, Greece.
authors.forename: Nikolaos
authors.initials: N
authors.lastname: Tsirigotakis
authors.affiliation: Laboratory of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine, University of Crete, Heraklion, Greece.
authors.forename: Emmanouil
authors.initials: E
authors.lastname: Dokianakis
authors.affiliation: Laboratory of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine, University of Crete, Heraklion, Greece.
authors.forename: Maria
authors.initials: M
authors.lastname: Antoniou
authors.affiliation: Veterinary Services of Cyprus, Nicosia, Cyprus.
authors.forename: Vasiliki
authors.initials: V
authors.lastname: Christodoulou
authors.affiliation: Veterinary Services of Cyprus, Nicosia, Cyprus.
authors.forename: Apostolos
authors.initials: A
authors.lastname: Mazeris
authors.affiliation: Department of Parasitology, Ege University, Izmir, Turkey.
authors.forename: Mehmet
authors.initials: M
authors.lastname: Karakus
authors.affiliation: Department of Parasitology, Ege University, Izmir, Turkey.
authors.forename: Yusuf
authors.initials: Y
authors.lastname: Ozbel
authors.affiliation: Vocational School of Health Sciences, Cela Bayar University, Manisa, Turkey.
authors.forename: Suha K
authors.initials: SK
authors.lastname: Arserim
authors.affiliation: Department of Biology, Ecology Division, HUESRL-VERG laboratories, Hacettepe University, Ankara, Turkey.
authors.forename: Ozge
authors.initials: O
authors.lastname: Erisoz Kasap
authors.affiliation: Department of Biology, Ecology Division, HUESRL-VERG laboratories, Hacettepe University, Ankara, Turkey.
authors.forename: Filiz
authors.initials: F
authors.lastname: Gunay
authors.affiliation: Department of Biology, Ecology Division, HUESRL-VERG laboratories, Hacettepe University, Ankara, Turkey.
authors.forename: Gizem
authors.initials: G
authors.lastname: Oguz
authors.affiliation: Veterinary Faculty, Mehmet Akif Ersoy University, Burdur, Turkey.
authors.forename: Sinan
authors.initials: S
authors.lastname: Kaynas
authors.affiliation: National Center for Disease Control and Public Health, Tbilisi, Georgia.
authors.forename: Nikoloz
authors.initials: N
authors.lastname: Tsertsvadze
authors.affiliation: National Center for Disease Control and Public Health, Tbilisi, Georgia.
authors.forename: Lamzira
authors.initials: L
authors.lastname: Tskhvaradze
authors.affiliation: National Center for Disease Control and Public Health, Tbilisi, Georgia.
authors.forename: Ekaterina
authors.initials: E
authors.lastname: Giorgobiani
authors.affiliation: M.I.P.I. Department, Unit of Vector-borne Diseases and International Health, Istituto Superiore di Sanità, Rome, Italy.
authors.forename: Marina
authors.initials: M
authors.lastname: Gramiccia
authors.affiliation: Department of Parasitology, Faculty of Science, Charles University, Prague, Czech Republic.
authors.forename: Petr
authors.initials: P
authors.lastname: Volf
authors.affiliation: M.I.P.I. Department, Unit of Vector-borne Diseases and International Health, Istituto Superiore di Sanità, Rome, Italy.
authors.forename: Luigi
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authors.lastname: Gradoni
mesh_terms: D000818:Animals; D002980:Climate; D005260:Female; D006801:Humans; D007303:Insect Vectors / Q000469:parasitology / Q000502:physiology*; D018314:Leishmania infantum / Q000502:physiology*; D007896:Leishmaniasis / Q000453:epidemiology / Q000469:parasitology / Q000635:transmission*; D008297:Male; D019083:Mediterranean Region / Q000453:epidemiology; D011157:Population Dynamics; D011576:Psychodidae / Q000469:parasitology / Q000502:physiology*; D012621:Seasons