ABOUT THE PRESENCE
OF PHLEBOTOMUS SERGENTI PARROT, 1917 (DIPTERA: PSYCHODIDAE) IN EASTERN SICILY, ITALY
D ' U R S O V.*, R U T A F.*. K H O U R Y C**, B I A N C H I R.**, D E P A Q U I T J.*** & M A R O L I M.**
Summary:
The note reports the data of a three-year sand fly investigation (1997-99) carried out in Eastern Sicily (Italy) with the aim to study the distribution of Phlebotomus sergenti. The survey involved a densely inhabited area at the foot of Mount Etna and the area of Iblei mounts. A total of 9,095 sand flies, of which 63.4 % males, were captured. Five species belonging to the genus Phlebotomus (P. perniciosus, P. perfiliewi, P. neglectus, P. sergenti and P. papatasi) and one to the genus Sergentomyia (S. minuta) were identified. Both the prevalence and distribution of the species were different within the two areas studied. In Mount Etna area, P. perniciosus [77.7 %) was the prevalent species followed by S. minuta (19.8 %), P. sergenti (2.0 %), P. neglectus (0.3 %) and P. papatasi (0.2 %). While in Iblei mounts region S. minuta (84,5 %) showed the highest prevalence, followed by P. perniciosus (14.4 %), P. perfiliewi (0,9 %) and P. neglectus (0,1 %). Here, P. sergenti was a very rare species (< 0.02).
P. sergenti was mostly associated to domestic habitats of peri- urban and urban zones located between two and 7 5 0 m a.s.l.
The density values of P. sergenti. expressed as number of
specimens/m2 of sticky trap, were between 0.3 and 5.5 with the highest value in the hilly collecting sites. The low observed abundance of P. sergenti does not allow to draw any prediction on the role that the species could play in the transmission of leishmaniasis in Sicily.
KEY WORDS : Phlebotomus sergenti. distribution, cutaneous leishmaniasis, Sicily, Italy.
Résumé :
SUR LA PRÉSENCE DE PHLEBOTOMUS SERGENTI PARROT,1917
(DIPTERA: PSYCHODIDAE) DANS L'EST DE LA SICILE (ITALIE) Les auteurs rapportent les résultats d'une enquête entomologique menée durant trois années (1997-1999) à l'aide de pièges adhésifs dans l'est de la Sicile (Italie) avec l'objectif d'étudier la distribution de Phlebotomus sergenti dans une région très peuplée au pied de l'Etna et dans celle des Monts Iblei. 9095 phlébotomes ont été capturés parmi lesquels 63,4 % de mâles. Cinq espèces appartenant au genre Phlebotomus (P. perniciosus, P. perfiliewi, P. neglectus, P. sergenti et P. papatasi) et une appartenant au genre Sergentomyia (S. minuta) ont été identifiées. La prévalence et la distribution de ces espèces varient selon la zone prospectée. Dans la région de l'Etna, P. perniciosus est l'espèce la plus abondante ( 7 7 , 7 %l suivie dans l'ordre décroissant par S. minuta (19,8 X), P. sergenti (2 %), P. neglectus (0,3 %) et P. pepatasi (0,2 %). Dans la zone des Monts Iblei, S. minuta est l'espèce la plus abondante (84,5 %l suivie par P. perniciosus (14,4 %), P. perfiliewi (0,9 %), P. neglectus (0, 1 %) et P. sergenti, extrêmement rare dans cette zone (< 0,02 %). Cette dernière espèce est presque toujours associée à des habitats domestiques en zone urbaine ou péri- urbaine, à des altitudes comprises entre deux et 750 mètres. Les densités observées varient entre 0,3 et 5,5 P. sergenti par mètre carré de papier huilé, les abondances les plus élevées étant corretees aux reliefs accidentés. Ces faibles abondances ne permettent aucune prédiction quant au rôle joué par P. sergenti en Sicile dans la transmission de Leishmania tropica. Néanmoins, sa distribution et son abondance en Sicile et dans le sud de la péninsule italienne devraient être évaluées périodiquement ainsi que la dynamique populationnelle et son anthropophilie.
MOTS CLES :
Phlebotomus sergenti, distribution, leishmaniose cutanée, Sicile, Italie.INTRODUCTION
P h e h o t o m u s sergenti Parrot, 1917 is r e c o r d e d in many countries o f the Mediterranean basin inclu- ding Western E u r o p e and Northern Africa. T h e hypothesis o f its migration from Central Asiatic regions a n d s u b s e q u e n t c o l o n i z a t i o n o f the Mediterranean
* Department of animal biology. University of Catania, Italy.
** MIPI department. Section of vector-borne diseases and interna- tional health, ISS, Rome, Italy.
*** Faculté de pharmacie, Université de Reims Champagne-Ardenne.
France.
Correspondence: Michèle Maroli.
Tel.: ++39 06 -19902302 - Fax: ++39 06 49387065 - E-mail: maroli@iss.it
regions has b e e n recently well d o c u m e n t e d by D e p a - quit et al. ( 2 0 0 2 ) . P. sergenti is well k n o w n to b e involved in the transmission o f L. tropica in Saudi Arabia (Al-Zahrani et al., 1 9 8 8 ) , M o r o c c o (Guilvard et al., 1 9 9 1 ) and Ethiopia ( G e b r e - M i c h a e l et al., 2 0 0 4 ) . It is s u s p e c t e d to b e the most p r o b a b l e vector in all the foci o f CL due to L. tropica (Killick-Kendrick, 1990;
Killick-Kendrick et ai, 1 9 9 5 ; Volf et al., 2 0 0 2 ) , e x c e p t in s o m e foci from East Africa and Namibia.
In Italy, P. sergenti has b e e n reported in the past only from a few localities o f Eastern Sicily (Adler & Theodor,
1931; B i o c c a et al., 1977). T h e present n o t e reports the data o f a three-year e n t o m o l o g i c a l survey ( 1 9 9 7 - 1 9 9 9 ) aimed to study the distribution o f P. sergenti in Eas- tern Sicily.
P a r a s i t e . 2 0 0 4 . 11, 2 7 9 - 2 8 3
M é m o i r e 2 7 9
Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/2004113279
MATERIALS A N D METHODS
STUDY AREA
S
icily is the largest island ( 2 5 . 4 2 6 k m2) in the Mediterranean basin. In Eastern Sicily, the highest mountain is Mount Etna ( 3 , 3 4 0 m . ) , the biggest v o l c a n o in Europe, rising b e t w e e n the Catania plain and the Simeto and Alcantara river valleys and the Sicilian A p e n n i n e s . S p o n t a n e o u s vegetation on the coastal areas consists o f the evergreen Mediterranean shrubs.
The most d e n s e l y populated areas are the coastal belt near Catania and Messina, around Palermo, Syracuse and the hinterlands o f Agrigento and Licata; the inland under populated areas include the highlands o f the Sicilian Apennines, the Etna, the Erei, the Iblei and other high g r o u n d in the west. T h e e n t o m o l o g i c a l survey was carried out in two different areas in the Eas
tern region. T h e first area w a s the densely inhabited z o n e at the foot o f Mount Etna including ten c o m munes o f Catania province and the s e c o n d was the Iblei mounts region, with six c o m m u n e s located in Syracuse province, four o f which w e r e hilly and two coastal, three c o m m u n e s in Ragusa province ( o n e o f which coastal) and o n e hilly c o m m u n e (Vizzini) in pro
vince o f Catania.
SAND FLY COLLECTIONS AND IDENTIFICATION Thirty collecting sites, containing a variety o f sand fly diurnal resting sites in rural, urban and peri-urban areas, w e r e selected throughout the two z o n e s under study (Fig. 1). Characteristics o f e a c h site and a list o f available hosts within a 5 0 m radius are presented in T a b l e I.
Sand fly specimens were collected by Lising sticky traps (20 x 20 c m ) , s o a k e d in castor oil and left in situ for
Fig. 1. - M a p o f E a s t e r n Sicily .showing t h e d i s t r i b u t i o n o f t h e c o l l e c t i n g sites ( 1-30). T h e c o m m u n e a n d t h e l o c a l i t y o f e a c h site a r e r e p o r t e d in T a b l e 1.
280 M é m o i r e P a r a s i t e , 2 0 0 4 , 11. 2 7 9 - 2 8 3
PHLEBOTOMUS SERGENTI IN SICILY
three nights. T w i c e mounthly collections w e r e carried out during a seven-mounth period (May-November) for three c o n s e c u t i v e years ( 1 9 9 7 - 1 9 9 9 ) . Collected speci
m e n s w e r e identified by their m o r p h o l o g i c a l charac
teristics a c c o r d i n g to T h e o d o r ( 1 9 5 8 ) and Leger et al.
( 1 9 8 3 ) . In particular, the identification o f male P. ser- genti s p e c i m e n s w a s b a s e d on the aspect o f the basal
process o f the c o x i t e w h i c h is curved and narrow (Fig. 2A) and on the n u m b e r ( < 2 2 ) o f its setae ( D e p a - quit et al., 1998). T h e globulous style showed two distal spines implanted at the s a m e level (Fig. 2 B ) . For fema
les, the identification was b a s e d on the number o f rings o f the s p e r m a t h e c a (five o r less) and the well d e v e loped pharyngeal armature. Moreover, the s e q u e n c i n g
Site
No. Commune Locality
Altitude
IN a.s.l. Zone Habitat Hosts
Etna area (CT)
1
Acireale Pozzillo
20IR do Humans, dogs, cats, rodents, lizards
2
Acireale S.M. La Scala
2 РЕdo Humans, dogs. cats, rodents, lizards
3
Acireale Piano d Api
280 РЕdo Humans, dogs. cats. pigs, chickens, rodents, lizards
4
Acicastello La Scogliera
5 РЕdo Humans, dogs, cats, rodents, lizards
5
Acicastello Ficarazzi
180 РЕdo Humans, dogs. cats, chickens, rodents, lizards
6
Tremestieri Nuovaluce
140UR do Humans, dogs, cats, rodents, lizards
7
S. Gregorio Guardiola Cantarella
280RU \vi Dogs, sheep, rodents, lizards
8
Trecastagni Pizzo Ferro
550 РЕdo Humans, dogs, chickens, rabbits, rodents, reptiles
9
Mascalucia Via Caravaggio
600 14'do Humans, dogs, rodents, lizards
10
Nicolosi Cemetery
700 РЕpe Humans, rodents, lizards
11
Nicolosi Ragala
750RU do Humans, dogs, cats, chickens, rodents, lizards
12
Belpasso Kennel
.300RU pi Humans, dogs, rodents, lizards
13
Zafferana Case Salenti
600 РЕpe Humans, dogs, cats, rodents, lizards
14
Maletto Balze Soprane
800 R1pi Humans, dogs, sheep, rodents, lizards Iblei area (SR-CT-RG)
15
Augusta Brucoli Adonai
20 R1pe Humans, dogs, cattle, rodents, lizards
16
Augusta Brucoli Puzzillo
2 РЕpe Humans, clogs, cattle, rodents, lizards
17
Siracusa City
10 1К do Humans, dogs, cats, rodents, lizards
18
Augusta Vignale
50RI' do Humans, dogs, rodents, lizards
19
Melilli Cugnicello
320RU wi Dogs, cattle, chickens, rodents, lizards
20
Melilli Pagliarazzi
430RU do Humans, dogs, cats, cattle, chickens, rodents, lizards
21
Melilli S. Giorgio
375RI wi Humans, dogs, rabbits, cattle, rodents, lizards
22
Melilli Cavittula
160 РЕdo Humans, dogs, cats, rodents, lizards
23
Sonino Mount Climite
430 RI\\ i Humans, dogs, cattle, sheep, rodents, lizards
2
I Sonino Town
438 1К pe Humans, dogs, cats, rodents, lizards
25
Feria Town
S58IR do Humans, dogs, cats, rodents, lizards
26
Bue I Iteri Town
895IR do Humans, dogs, cats, rodents, lizards
Г Vizzini Periphery
619 РЕpe Humans, dogs, rodents, lizards
28
Chiaramounte Gulfl Town
668UR do Humans, dogs, rodents, lizards
29
Mounterosso Almo Town
690 1li do Humans, dogs, rodents, lizards
30
Marina ili Ragusa Town
5 1К do Humans, dogs, cats, rodents, lizards
CT, C a t a n i a ; S R . S i r a c u s a ; R G . R a g u s a ; UR, u r b a n ; P E . p e r i - u r b a n ; RU, rural; d o , d o m e s t i c ; p e , p e r i - d o m e s t i c ; w i , w i l d .
T a b l e I. - C h a r a c t e r i s t i c s o f t h e c o l l e c t i n g sites m o n i t o r e d in E a s t e r n Sicily ( 1 9 9 7 - 1 9 9 9 ) ; locality, altitude, h a b i t a t a n d list o f a v a i l a b l e h o s t s w i t h i n a 5 0 m radius.
Fig. 2 . - B a s a l p r o c e s s o f t h e c o x i t e ( A ) a n d style ( B ) o f a Sicilian P. SERGENTI.
2 8 1 P a r a s i t e , 2 0 0 4 . 11, 2 7 9 - 2 8 3
M é m o i r e
o f the s e c o n d internal transcribed s p a c e r o f the ribo- somal DNA o f o n e Sicilian s p e c i m e n ( G e n b a n k a c c e s sion n u m b e r AF 4 6 2 3 3 0 ) e m p h a s i s e d without doubt its identity: P. sergenti ( D e p a q u i t et al., 2 0 0 2 ) .
RESULTS A N D DISCUSSION
T
h e n u m b e r o f sand flies c o l l e c t e d in e a c h site and the p r e v a l e n c e values for the s p e c i e s identified are reported in T a b l e II. Overall, 9 , 0 9 5 sand flies s p e c i m e n s , o f w h i c h 63-4 % w e r e males, w e r e captured during the three-year study. Five spe
cies b e l o n g i n g to the g e n u s Pblebotomus Rondani and Berte, 1 8 4 0 (P. perniciosus, P. perfiliewi, P. neglectus T o n n o i r , 1 9 2 1 , P. sergenti and P. papatasi (Scopoli, 1 7 8 6 ) ) and o n e to the genus Sergentomyia Franca &
Parrot, 1 9 2 0 (S. minuta (Rondani, 1 8 4 3 ) ) w e r e identi
fied.
O n t h e w h o l e , t h e m o r e a b u n d a n t s p e c i e s w e r e S. minuta ( 6 3 . 5 % ) and P. perniciosus ( 3 5 . 0 % ) . T h e
other s p e c i e s identified s h o w e d p e r c e n t a g e value less than 1 %. Among those, P. sergenti was the most abun
dant (0.7 % ) . B o t h the p r e v a l e n c e and distribution o f the sand fly species w e r e different within the two areas studied ( T a b l e II). In the Etna area, P. perniciosus (77.7 % ) was the most abundant followed b y 5. minuta ( 1 9 . 8 % ) , P. sergenti ( 2 . 0 % ) , P. neglectus ( 0 . 3 % ) and P. papatasi ( 0 . 2 % ) . In the less anthropized and dry area o f Iblei mounts, the s p e c i e s s h o w e d a different p r e v a l e n c e , b e i n g S. minuta ( 8 4 . 5 % ) the most w i d e s pread s p e c i e s . In this area, a m o n g the Pblebotomus genus, the s p e c i e s s h o w e d the following p r e v a l e n c e : P. perniciosus ( 1 4 . 4 % ) , P. perfiliewi ( 0 . 9 % ) , P. neglec
tus (0.1 % ) . P. sergenti w a s very rare b e i n g only o n e s p e c i m e n c o l l e c t e d from a rural site l o c a t e d at 4 2 0 m a.s.l. T h e trend o f seasonal activity o f p h l e b o t o m i n e s varied during the three years, being adult flies collected b e t w e e n May-November o f e a c h year.
From previous entomological investigations carried out in Sicily at the e n d o f '80, it appears that P. sergenti is apparently absent in western and the central areas
No. Total P. perniciosus P. neglectus P. sergenti P. perfiliewi P. papatasi P. minuta
Etna area
1 428 380 (88.8) 2 (0.5) 12 (2.8) - 1 (0.2) 33 (7.7)
2 32 26 (81.3) - 1 (3.1) - - 5 (15.6)
3 12 8 (66.6) - 2 (16.7) - - 2 (16.7)
4 21 19 (90.5) - - - - 2 (9.5)
5 1,154 991(85.9) 1 (0.1) 20 (1.7) - 5 (0.4) 137 (11.9)
6 23 20 (87.0) - - - - 3 (13.0)
7 350 130 (37.1) - - - - 220 (62.9)
8 120 83 (69.1) 1 (0.9) 9 (7.5) - - 27 (22.5)
9 172 92 (53.5) 3 (1.8) 12 (6.9) - - 65 (37.8)
10 16 7 (43.7) - - - 9 (56.3)
11 129 85 (65.9) 2 (1.5) 1 (0.8) - _ 41(31.8)
12 465 451 (97.1) 1 (0.2) 3 (0.6) - - 10 (2.1)
13 34 6 (17.7) - - - - 28 (82.3)
14 6 3 (50) 1 (16.7) - - - 2 (33.3)
Total 2,962 2,301 (77.7) 11 (0.3) 60 (2.0) - 6 (0.2) 584 (19.8)
Iblei area
15 662 234 (35.3) 2 (0.3) - - - 426 (64.4)
16 3,528 508 (14.4) - - 56 (1.6) - 2,964 (84)
17 20 6 (30) - - - - 14 (70)
18 14 - - - - - 14 (100)
19 36 11 (30.5) - - - - 25 (69.5)
20 529 15 (2.8) - 1 (0.2) 1 (0.2) - 512 (96.8)
21 159 6 (3.8) 1 (0.6) - - - 152 (95.6)
22 1,045 89 (8.5) 2 (0.2) - - - 954 (91.3)
23 5 - - - 5 (100)
2) 2 1 (50) - - - - 1 (50)
2S 16 3 (18.8) - - - - 13 (81.2)
26 5 - - - 5 (100)
27 107 8 (7.5) - - - - 99 (92.5)
28 1 - - - 1 (100)
29 3 1 (33.3) - - - - 2 (66.7)
30 1 - - - - - 1 (100)
Total 6,133 882 (14.4) 5 (0.1) 1 (< 0.02) 57 (0.9) - 5,188 (84.5)
Overall 9,095 3,183 (35) 16 (0.1) 61 (0.7) 57 (0.6) 6 (< .00.1) 5,772 (63.5) Table II. - Number and percentages of phlebotomine species identified from 30 collecting sites in Eastern Sicily during the sand fly sea
sons 1997-1999.
2 8 2 Mémoire P a r a s i t e , 2 0 0 4 , 11, 2 7 9 - 2 8 3
PHLEBOTOMUS SERGENTI IN SICILY
o f this island (Ansaldi et al, 1 9 9 0 ; Maroli et al, 1 9 8 8 , 1 9 9 0 ) . O u r data confirm the p r e s e n c e o f P. sergenti in Eastern Sicily a n d s h o w that it is widespread at the foot o f Mount Etna, b e i n g found in 57.1 % o f t h e collec- ting sites studied in this area. T h e s p e c i e s w a s mostly associated to domestic habitats o f peri-urban and urban z o n e s located b e t w e e n t w o a n d 7 5 0 m a.s.l. T h e den- sity values o f P. sergenti, e x p r e s s e d as n u m b e r speci- m e n s / m2 o f sticky trap, w e r e b e t w e e n 0.3 a n d 5.5 with the highest value in the hilly collecting sites.
T h e present work has pointed out that in Eastern Sicily P. sergenti c o u l d easily c o l o n i z e d o m e s t i c habitats w h e r e it is in close contact with h u m a n s a n d domestic animals. It could b e argued that its present a b u n d a n c e is unable to play any role in the epidemiology o f leish- maniasis in Sicily. Nevertheless its p r e s e n c e in the big- gest island o f the Mediterranean basin is o f particular importance in view o f several factors. Sicily is a bridge b e t w e e n Europe a n d North Africa. O n this subject it is worthy to mention that Depaquit et al. ( 2 0 0 2 ) , b y stu- dying intraspecific variations o f different geographical populations o f P. sergenti, has observed that Sicilian and M o r o c c a n strains a p p e a r to b e sister p o p u l a t i o n s . Besides, in M o r o c c o a recent investigation has shown that P. sergenti is highly susceptible to L. tropica (Rioux, 2 0 0 1 ) . Therefore, considering all the above, there could b e a potential risk o f L. tropica introduction to Sicily.
So, it will b e useful to continue the monitoring o f P. ser- genti in Sicily a n d in southern Italy in order to define its future range o f dispersion. Morover, in the neigh- bouring villages o f the Etna zone, a study o f the popu- lation dynamics and biting activity o f the species in rela- tion to the role played on Leisbmania transmission should b e w e l c o m e .
REFERENCES
ADLER S. & THEODOR O. Investigations on Mediterranean kala azar. III. - The sandflies of the Mediterranean basin. Dis- tribution and bionomics of sandflies in Catania and dis- trict. Proceedings of the Royal Society of London (B), 1931, 108, 464-480.
AL-ZAHRANI M.A., PETERS W . , EVANS D.A., CHIN C , SMITH V . &
LAXE R.P. Phlebotomus sergenti, a vector of Leishmania tro- pica in Saudi Arabia. Transactions of the Royal Society of
Tropical Medicine and Hygiene, 1988, 82, 416.
ANSALDI G., LAVAGNINO A., LIBRIZZI R. & MAROLI M. Flebotomi antropofili in Sicilia occidentale: osservazione sulla distri- buzione. Rivista di Parassitologia, 1990, 51, 217-219.
BIOCCA E . , COLUZZI A. & CONSTANTINI R. Osservazioni sulla attuale distribuzione dei flebotomi italiani e su alcuni caratteri morfologici differenziali tra le secie del sottoge- nere Phlebotomus (Larroussius). Parassitologia, 1977, 19, 19-31.
DEPAQUIT J . , FERTÉ H . , LÉGER N., LEFRANC F . , ALVES-PIRES C , HANAFI H . , MAROU M., MORILLAS-MÁRQUEZ F . , RIOUX J.A., Svo-
BODOVA M. & VOLF P. ITS 2 sequences hetergeneity in Phle- botomus sei-genti Parrot, 1917 and Phlebotomus similis: pos- sible consequence in their ability to transmit Leishmania tropica. International Journal for Parasitology, 2002, 32, 1123-1131.
DEPAQUIT J . , LÉGER N. & FERTÉ. H. Le statut taxinomique de Phlebotomus sergenti Parrot, 1917, vecteur de Leishmania tropica (Wright, 1903) et Phlebotomus similis Perfiliev, 1963 (Diptera-Psychodidae). Approches morphologique et mor- phométrique. Corollaires biogéographiques et épidémio- logiques. Bulletin de la Société de Pathologie Exotique.
1998, 91, 346-352.
GEBRE-MICHAEL T . , BALKEW M., ALI A., LUDOVISI A. & GRAMIC- CIA M. The isolation of Leishmania tropica and L. aethio- pica from Phlebotomus (Paraphlebotomus) species (Dip- tera-Psychodidae) in the Awash Valley, northearn Ethiopia.
Transactions of the Royal Society of Tropical Medicine and Hygiene, 2004, 98, 64-70.
GUILVARD E., RIOUX J . A., GALLEGO M., PRATLONG F., MAHJOUR J . , MARTINEZ-ORTEGA E., DEREURE J . , SADDIKI A. & MARTINI A.
Leishmania tropica au Maroc III. Rôle vecteur de Phlebo- tomus sergenti. Annales de Parasitologic Humaine et Com- parée, 1991, 66, 96-99.
KILLICK-KENDRICK R. Plebotomine vectors of the leishmania- sies: a review. Medical and Veterinary Entomology, 1990, 4, 1-24
KILLICK-KENDRICK R., KILLICK-KENDRICK M. &. TANG Y. Anthro- ponotic cutaneous leishmaniasis in Kabul, Afghanistan: the high susceptibility of Phlebotomus sergenti to Leishmania tropica. Transactions of the Royal Society of Tropical Medi- cine and Hygiene, 1995, 89, 477.
LÉGER N., PESSON B . , MADULO-LEBLOND G . & ABONNENC E. Sur la différenciation des femelles du sous-genre Larroussius Nitzulescu, 1931 (Diptera-Phlebotomidae) de la région médi- terranéenne. Annales de Parasitologic Humaine et Com- parée, 1983, 58, 611-623.
MAROLI M., LAVAGNINO A., ANSALDI G . & CAVALLINI C. Indagine sui vettori di leishmaniosi (Diptera, Psychodidae) in tre dif- ferenti ambienti della Sicilia occidentale e in due delle isole Eolie. Parassitologia, 1990, 32, 305-311.
MAROLI M., PAMPIGLIONE S. & TOSTI A. Cutaneous leishmaniasis in western Sicily (Italy) and preliminary survey of phle- botomine sandflies (Diptera: Psychodidae). Parassitologia, 1988, 30, 211-217.
RIOUX J.A. Trente ans de coopération franco-marocaine sur les leishmanioses : dépistage des foyers. Facteurs de ris- que. Changements climatiques et dynamique noso-géogra- phique. Bulletin de lAssociation des Anciens Élèves de l'Ins- titut Pasteur, 2001, 168, 90-101.
THEODOR O . Psychodidae-Phlebotominae. Die Fliegen der Palaearktischen Region, 1958, 9c, 1-55.
VOLF P., OZBEL Y., AKKAFA F., SVOBODOVA M., VOTYPKA J . &
CHANG K.P. Sand flies (Diptera: Phlebotominae) in San- liurfa, Turkey: relationship of Phlebotomus sergenti with the epidemic of anthroponotic cutaneous leishmaniasis.
Journal of Medical Entomology, 2002, 39, 12-15
Reçu le 20 octobre 2003 Accepté le 16 avril 2004 Parasite, 2 0 0 4 , 11, 2 7 9 - 2 8 3
M é m o i r e 283
