A Two-Year Survey on Mosquitoes of Lebanon Knio K.M.*, Markarian N.*, Kassis A.* & Nuwayri-Salti N.**

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A Two-Year Survey on Mosquitoes of Lebanon Knio K.M.*, Markarian N.*, Kassis A.* & Nuwayri-Salti N.** Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/2005123229 A TWO-YEAR SURVEY ON MOSQUITOES OF LEBANON KNIO K.M.*, MARKARIAN N.*, KASSIS A.* & NUWAYRI-SALTI N.** Summary: Résumé : LES MOUSTIQUES DU LIBAN : RÉSULTATS DE DEUX ANS DE RÉCOLTES A total of 6,500 mosquitoes were identified during a two-year survey (1999-2001) in Lebanon, and these belonged to twelve Au cours d’une période d’observation de deux ans (1999-2001), species: Culex pipiens, Cx. laticinctus, Cx. mimeticus, 6500 moustiques ont été identifiés au Liban et répartis en Cx. hortensis, Cx. judaicus, Aedes aegypti, Ae. cretinus, 12 espèces : Culex pipiens, Cx. laticinctus, Cx. mimeticus, Ochlerotatus caspius, Oc. geniculatus, Oc. pulchritarsis, Culiseta Cx. hortensis, Cx. judaicus, Aedes aegypti, Ae. cretinus, longiareolata and Anopheles claviger. Culex pipiens was the most Ochlerotatus caspius, Oc. geniculatus, Oc. pulchritarsis, Culiseta predominant species in Lebanon, collected indoors and outdoors. longiareolata and Anopheles claviger. Culex pipiens, l’espèce It was continuously abundant and active throughout the year. prédominante, a été collectée à l’extérieur et à l’intérieur. Elle a Culex judaicus was a small and rare mosquito and it is reported été trouvée abondante et active tout au long de l’année. Culex to occur for the first time in Lebanon. On the coastal areas, judaicus, espèce petite et rare, a été observée et identifiée pour Ochlerotatus caspius was very common, and proved to be a la première fois au Liban. Dans les zones côtières, il s’est avéré complex of species as two forms were detected. One of the que l’espèce Ochlerotatus caspius, très communément observée, vectors of malaria, Anopheles claviger, was collected from May to était en fait un complexe car deux formes ont été identifiées. September, from eight sites in Lebanon. Its breeding sites were Anopheles claviger, porteur de malaria, a été collecté de mai à restricted to fresh, cool, and clean water in pools and wells. Most septembre sur huit sites libanais. Leur habitat de prédilection était of these breeding sites were in the populated Metn County where l’eau claire et froide des puits et bassins. La plupart des sites a few indigenous cases of malaria were reported from 1997- concernés se trouvent dans le comté du Metn où quelque cas de 2000. This shows that the reported malaria cases were not malaria autochtones ont été rapportés entre 1997 et 2000, ceci imported, but caused by the bites of locally infected Anopheles prouvant bien l’implication des anophèles femelles localement females. infectées. KEY WORDS : mosquito, Culex, Anopheles, malaria, Lebanon. MOTS CLÉS : moustique, Culex, Anopheles, paludisme, Liban. osquitoes are of great economic importance In Lebanon, several mosquito-borne diseases mainly because many act as vectors for a number of malaria and dengue were endemic until the 1950’s Mhuman diseases, such as malaria, dengue, when the government launched a mosquito eradica- filariasis, and several types of encephalitis including tion program (Matossian & Ibrahim, 1974). No cases West Nile fever (Service, 1993). With the constantly of dengue and malaria were reported afterward; changing environment, the epidemiology of mosquito- however, since 1997, several incidences of local malaria borne diseases is also modified. Global warming, per- have occurred in some populated areas of Lebanon iodic flooding and deforestation have opened new (Hamadeh, 1997). It seems that malaria still poses a habitats to mosquitoes which show high plasticity in threat to the country especially that the disease was their breeding behavior and readily spread their dis- never eradicated from the neighboring countries. To tribution. In fact, sporadic malaria outbreaks have examine the transmission of diseases by mosquitoes been reported in non-endemic countries and trans- in Lebanon, it is critical to start by studying the taxo- mission of the disease was caused by the bite of a nomy, distribution and abundance of these vectors, locally infected Anopheles species (Zucker, 1996). especially that knowledge of the mosquito species in Lebanon is very patchy and dates from the 1940’s and * Biology Department, Faculty of Arts & Sciences, American Uni- 70’s (Parr, 1943; Matossian & Ibrahim, 1974). versity of Beirut, Beirut, Lebanon. The aims of this study are to update and evaluate the ** Department of Human Morphology, Faculty of Medicine, Ame- current status of mosquito species in Lebanon, and to rican University of Beirut, Beirut, Lebanon. determine the breeding sites, abundance and distri- Correspondence: Dr Khouzama Knio. Tel.: 961 350 000 (ext. 3886) – Fax: 961 1 351706. bution of the Lebanese mosquitoes, with special E-mail: [email protected] emphasis on the malaria vectors. Parasite, 2005, 12, 229-235 Mémoire 229 KNIO K.M., MARKARIAN N., KASSIS A. & NUWAYRI-SALTI N. MATERIALS AND METHODS In order to estimate changes in mosquito density throughout the year, periodic indoor house collections from July 1999 to July 2000 were made weekly in five tarting 1999, a two-year survey on mosquito spe- selected houses situated in Beirut and its suburbs: Ain cies was initiated in Lebanon. Mosquitoes were El Roumaheh (Greater Beirut), Sabtieh (Greater Beirut), collected from all provinces and sectors of the S Zalka (Metn Co., Mount Lebanon), Nabay (Metn Co., country, with the exception of some inaccessible areas Mount Lebanon), and Rabwe (Metn Co., Mount Leba- in the South (Fig. 1). The aquatic larvae and pupae non). The weekly indoor collections involved the same were collected using dippers (Bioquip), from different catch efforts per unit time in each house: number of breeding sites, such as rocky pools, ponds, swamps, actively biting and resting mosquitoes caught during irrigation ditches, streams... They were brought to the five hours after sunset. laboratory and reared into adults using mosquito bree- The taxonomy of the collected mosquitoes were deter- ders (Bioquip). mined using keys by Dubose & Cutin (1965), Harbach Adult mosquitoes were collected from outdoors and (1985, 1988), Jayson (1992), Glick (1992), and Sama- indoors using various methods, such as vials, aspira- nidou-Voyadjoglou & Harbach (2001) after an initial tors, human bait technique, and mosquito traps (Stan- consultation and species confirmation by Dr Harbach dard New Jersey Light Trap, and Heavy Duty EVS CO2 (NHM, London). Voucher specimens were preserved Mosquito Trap by Bioquip). in the NHM, American University of Beirut. RESULTS total of 6,500 mosquitoes were collected from 1 various sites in Lebanon. The mosquitoes belon- North Tripoli Aged to two subfamilies, Culicinae and Anophe- linae, and twelve species: a - Culex (Culex) pipiens; 2 4 3 b-Cx. (Culex) laticinctus; c - Cx. (Culex) mimeticus; 5 d-Cx. (Maillotia) hortensis; e - Cx. (Neoculex) judai- Mediterranean 6 cus;f-Ochlerotatus (Ochlerotatus) caspius; g - Oc. (Fin- Sea 7 laya) geniculatus; h - Oc. (Ochlerotatus) pulchritarsis; Mount Beqaa i-Aedes (stegomyia) cretinus;j-Ae. (Stegomyia) aegypti; Lebanon 8 k-Culiseta (Allotheobaldia) longiareolata; and l - Ano- 16 Beirut 9 pheles (Anopheles) claviger. 10 The regions with GPS readings where different mos- 17 11 quito species were collected are indicated in the text below with the exception of Cx. pipiens which was Syria 12 extremely widespread in the country. For this reason, Saida 18 the counties and number of sites per county are indi- cated for the latter species. 13 South a - Culex (Culex) pipiens Linnaeus, 1758 15 Greater Beirut: 442F:15M Beirut (20 sites). Mount Leba- Tyr non: 597F:36M (Aaley Co.) (14 sites); 514F:12M 8.7 Km 14 (Baabdah Co.) (4 sites); 292F:18M (Chouf Co.) (12 sites); 385F:40M (Kesrouan Co.) (14 sites); 588F:31M (Metn Co.) (22 sites); 205F:2M (Jbeil Co.) (5 sites). North Leba- non: 78F (Batroun Co.) (2 sites); 274F:5M Koura (Co.) (6 sites); 112F:5M (Tripoli Co.) (4 sites); 10F:4M (Akkar Co.) (2 sites); 10F (Zgharta Co.) (2 sites). South Leba- Fig. 1. – Map of Lebanon showing the different counties where mos- non: 156F:10M (Saida Co.) (6 sites); 94F:2M (Nabatiyeh quitoes were collected for this survey, and showing the sites of col- Co.) (2 sites); 96F:4M (Tyr Co.) (4 sites). Beqaa Valley: lection of Anopheles claviger. (1) Akkar Co.; (2) Tripoli Co.; (3) Zgharta Co.; (4) Koura Co.; 172F:13M (Zahle Co.) (5 sites); 507F:12M (Baalback (5) Bcharre Co.; (6) Batroun Co.; (7) Jbeil Co.; (8) Kesrouan Co.; Co.) (6 ); 329F:12M (West Beqaa Co.) (4 sites). (9) Metn Co.; (10) Baabdah Co.; (11) Aaley Co.; (12) Chouf Co.; Culex pipiens was the most predominant and wides- (13) Saida Co.; (14) Tyr Co.; (15) Nabatiyeh Co.; (16) Baalback Co.; pread species in Lebanon, collected indoors and out- (17) Zahleh Co.; (18) West Beqaa Co. (• denotes sites of collection of An. claviger). doors, and comprising ca. 78 % of the total collected Parasite, 2005, 12, 229-235 230 Mémoire MOSQUITOES OF LEBANON Total behavior was anthropophilic, endophagic, and endo- Species number Females Males Percentage philic. In 1999-2000, the changes in population den- sity of Cx. pipiens indoors, as observed in the moni- Culex pipiens 5,082 4,861 221 78.20 tored houses, showed that the female mosquitoes were Cx. laticinctus 142 77 65 2.18 Cx. mimeticus 99 51 48 1.52 active throughout the year as long as the temperature Cx. hortensis 39 22 17 0.60 was favourable (Fig. 2). An increase in the population Cx. judaicus 33 22 11 0.51 of Cx. pipiens females was detected in November Ochlerotatus caspius 769 526 243 11.83 when the temperature started to drop. This could be Oc. geniculatus 20 20 – 0.31 Oc. pulchritarsis 2 2 – 0.03 explained by the fact that the females appeared to be Ae. cretinus 34 32 2 0.52 the overwintering stage, and remained active and did Ae. aegypti 1 – 1 0.01 not hibernate when the winter was wild.
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