About sand fliesSand flies are biting insects that share some similarities with mosquitoes, being classified in the suborder, the Nematocera. They are widely spread in regions with warm temperate through subtropical to tropical climates. The veterinary and medical importance of sand flies results from their ability to transmit viral, bacterial and protozoal diseases.

Sand flies belong to the insect order Diptera, suborder Nematocera. Within this suborder the family Psychodidae includes biting sand flies in diverse genera and non-biting owl-midges or moth flies (genus Psychoda). The subfamilyPhlebotominaeconsists of about 700 phlebotomine species. Among the existing phlebotomine genera two have been proven as vectors of one of the main zoonotic pathogens worldwide, the protozoan parasiteLeishmania. These arePhlebotomusin the Old World andLutzomyiain the New World.

Sand fly-transmitted diseasesare a major health issue for dogs. Even with preventative measures, mosquito control with repellent and insecticidal efficacy is crucial.

Figure 1:Adult sand fly (Phlebotomus spp.), frontal view (SEM)

TaxonomySand flies are members of the phylum Arthropoda and belong to the class of Insecta. This class is the largest group of animals with respect to the number of species (~773,000) and individuals. Among other characteristics, three body sections are typical of this class.

As mosquitoes, sand flies are members of the suborder Nematocera. Both members can be recognised by their many segmented antennae, which are usually long. Most of the nematocerans are small, slender and long-legged, usually midge- or mosquito-like in appearance.

Of the about 700 phlebotomine sand fly species, only about 70 are anthropophagous. Phlebotomines are able to transmit viral, bacterial and parasite diseases (Mehlhorn, 2001).

Within the suborder Nematocera, many flies are of economic importance, as pests or even disease vectors. The Nematoceran larvae possess a well-developed head, and most live in water or in moist habitat, being an important item in the food chain of many freshwater fishes as aquatic larvae.

The suborder Nematocera contains a little less than one-third of the North American species of flies, in 23 of the 105 families. Of the about 700 phlebotomine sand fly species, only about 70 are anthropophagous. Phlebotomines are able to transmit viral, bacterial and parasite diseases (Mehlhorn, 2001).

Phylum:Arthropoda

Subphylum:Tracheata (= Antennata)

Class:Insectea (= Insecta, Hexapoda)

Subclass:Pterygotia (flying insects; here a section with complete metamorphosis)

Order:Dipterida (i.e. two-winged insects)

Suborder:Nematocera

Family:Phlebotomidae / Psychodidae

Subfamily:Phlebotominae

Order

The order Diptera, i.e. two-winged flies, is including house-flies, stable-flies, blue-bottles, tsetse-flies and many others

The hind wings in this order are modified as the halteres, small organs that vibrate during flight and are believed to have a gyroscopic function providing a constant flight attitude.

Suborder

The suborder Nematocera is including midges, sand flies, black flies, mothflies, harlequin-flies and mosquitoes.

Family

The family Phlebotominae / Psychodidae includes biting sand flies in diverse genera (see below) and non-biting owl-midges or moth flies in the genusPsychoda.

The psychodids are small to minute, usually very hairy, moth-like flies that hold their wings roof-like over the body when resting. The adults occur in moist, shady places. These flies are sometimes highly abundant in drains or sewers. Their larvae occur in decaying vegetable matter, mud, moss, or water.

Subfamily and Genera

Within the subfamily Phlebotominae there are about 700 species of phlebotomine sand flies. The number of genera is depending on the hierarchical classification adopted, but according to the most widely accepted concept, six genera exist:Phlebotomus,SergentomyiaandChiniusin the Old World andLutzomyia,BrumptomyiaandWarileyain the New World. Only sand flies in the generaPhlebotomusandLutzomyiaare proven vectors ofLeishmania, though in other genera man-biting flies also occur.

Diverse subgenera within the different genera exist. An overview over different species with their according subgenera is listed below.

References

Mehlhorn, H.: Sand flies. In: Mehlhorn, H. (ed.): Encyclopedic reference of parasitology. Biology, structure, function. 2nd edn., Springer Verlag, Berlin, pp. 563-565, 2001EvolutionFossil phlebotomines are about 120 million years old (Mehlhorn, 2001).It has been suggested that sand flies existed before the continents separated and thatPhlebotomusevolved in the Old World but failed to reach North America because the Bering land bridge did not become warm enough (Perfil'ev, 1968).The genusLutzomyiaprobably is polyphyletic, i.e. of more than one evolutionary origin and may eventually have to be split (WHO, 1990).

References

Mehlhorn, H.: Sand flies. In: Mehlhorn, H. (ed.): Encyclopedic reference of parasitology. Biology, structure, function. 2nd edn., Springer Verlag, Berlin, pp. 563-565, 2001 Perfil'ev, P.P.: Fauna of U.S.S.R. Diptera.Phlebotomidae(sandflies). Acad. Sci. U.S.S.R. Zool. Inst. New Ser. No. 93, Vol. 3 No. 2, Israel Program for Scientific Translations, Jerusalem, 1968WHO: Control of the leishmaniases. Report of a WHO Expert Committee, Tech. Rep. Ser. No. 793, WHO, Geneva, 1990

EpidemiologyEssential for the epidemiology of any vector-borne disease is the vector-host contact. A quantitative assessment makes it possible to predict epidemiologically dangerous situations and to take adequate measures of prevention and vector control. The extent of contact is strongly influenced by the feeding habit of the vector and the availability and activity of the hosts at the place and time of vector activity (WHO, 1972). Examples for hosts coming into contact with vectors have been observed in road building in Panama or agricultural development in Costa Rica which has brought men into contact with sand flies which inhabit the tropical forests without normally having contact with man (Lewis, 1971).

Sand flies have a limited chance to find a host while the distance they can travel is short compared with some flies or even mosquitoes. They often move in short hops. Most of them remain within 20-30 cm of the soil surface.

Whereas the maximum flight distance ofPh. ariasiin trials in France has been 2.3 km (Killick-Kendrick et al., 1984). Flight speed inPh. ariasiwas estimated to be around 1m/sec (Killick-Kendrick et al., 1986).

Sand flies are usually not found at great altitudes, but have been reported as vector of the uta called form of dermal leishmaniosis at 2800 m (in Peru). Sand flies often stay close to the ground, but some American forests sand flies bite in the canopy, some at all levels or in a middle zone while following their hosts (Shaw et al. 1972).

References

WHO: Vector ecology. Report of a WHO Scientific Group, Tech. Rep. Ser. No. 501, WHO, Geneva, 1972 Lewis, D.J.: Phlebotomid sandflies. Bull. WHO 44, 535-551, 1971 Killick-Kendrick, R., J.-A. Rioux, M. Bailly, M.W. Guy, T J. Wilkes, F.M. Guy, I. Davidson, R. Knechtli, R.D. Ward, E. Guilvard, J. Prires and H. Dubois: Ecology of leishmaniasis in the south of France. 20. Dispersal ofPhlebotomus ariasiTonnoir, 1921 as a factor in the spread of visceral leishmaniasis in the Cvennes. Ann. Parasitol. Hum. Comp. 59, 555-572, 1984 Killick-Kendrick, R., T.J. Wilkes, M. Bailly, I. Bailly and L.A. Righton: Preliminary field observations on the flight speed of a phlebotomine sandfly. Trans. R. Soc. Trop. Med. Hyg. 80, 138-142, 1986Shaw, J.J., R. Lainson and R.D. Ward: Leishmaniasis in Brazil: VI. Observations on the seasonal variations ofLutzomyia flaviscutellata(Mangabeira) with particular reference to its biting habits at different heights. Trans. R. Trop. Med. Hyg. 66, 718-724, 1972

DistributionThe family Phlebotomidae is largely tropical with a mainly Palaearctic element, the genusPhlebotomus, which includes some tropical mammalophilic species. The Palaearctic region, which is the main temperate area of the Old World, is dominated by the genusPhlebotomus.

In the Old World sand flies tend to be more numerous in relatively dry zones. In the New World they favour the forests which cover much of the tropics. Thus they occur in warmer regions of temperate countries, e.g. Mediterranean countries, the Middle East, Africa, India and China, and in tropical countries. Of medical importance there,Lutzomyiaspecies are especially common in forested areas of Central and South America.

Old World

Phlebotomusis dominant in the Palaearctic region and extents into the other three zoogeographical regions of the Old World. In the former Soviet Union sand flies occur in the Mediterranean and Central Asian subzones of the Palaearctic region. They also have been reported from an area north of Paris and the Isle of Jersey. Savanna, steppe and desert are typical habitats in the Old World.Of the genusPhlebotomus, the sand flyPh. (Transphlebotomus) mascittiiGrassi, 1908 appears to be the most northerly species (Rioux et al., 1969).Lewis (1982) describes the distribution ofPhlebotomusnorthward to just above latitude 49 N. In 1999 supposedly for the first time a sand fly, namelyPh. mascittii, has been detected in Germany (Naucke and Pesson, 2000).

Distribution of phlebotomines as vectors of Leishmania in the Old World

Five criteria of incrimination have been stated by R. Killick-Kendrick, including corresponding epidemiological data, anthropophilic behaviour of the sandfly, promastigote isolation from the sandfly, complete life cycle of the parasite in the vector and experimental transmission by the bite of the infected species.Nine species of closely related sand flies classified in the genusPhlebotomus, subgenusLarrousius,are vectors of Mediterranean CanL. Of the causative organism,L. infantum, sufficient numbers of typed isolates have been cultured from five of the ninePhlebotomus(Larrousius) species (Ph. perniciosus;Ph. ariasi,Ph. perfiliewi,Ph. neglectus,Ph. langeroni), so their role as vectors considered as proven (Killick-Kendrick, 1990a; 1999b). The behaviour and ability ofPh. tobbito support the growth ofL. infantumin experimental conditions (Rioux et al, 1998) is taken as evidence for the vectorial role of this species. The remaining three speciesPh. longicuspis,Ph. kandelakiiandPh. syriacusare assumed to be probable vectors on circumstantial evidence, namely their distribution, biting habits and taxonomic position (Killick-Kendrick and Killick-Kendrick, 1999).

Vector speciesCountries around the Mediterranean basin

Ph. perniciosus*Portugal, Spain, France, Italy, Malta, Cyprus, Yugoslavia, Turkey, Syria, Morocco, Algeria, Tunisia, Libya

Ph. ariasi*Portugal, Spain, France, Italy, Morocco, Algeria, Tunisia

Ph. perfiliewispp.*Italy, Malta, Cyprus, Greece, Israel, Yugoslavia, Morocco, Algeria, Tunisia

Ph. longcuspisMorocco, Algeria, Tunisia, Libya, Spain

Ph. neglectus*Italy, Greece, Yugoslavia, Albania

Ph. tobbiItaly (Sicily), Cyprus, Greece, Yugoslavia, Turkey, Lebanon, Israel, Syria

Ph. kandelakiiLebanon, Turkey

Ph. syriacusIsrael, Jordan, Syria

Ph. langeroni*Morocco, Algeria, Tunisia, Libya?, Egypt, Spain

Table: Distribution of the proven and probable phlebotomine vectors, (subgenusLarroussius) of CanL around the Mediterranean basin (from maps of Lewis, 1982) (Killick-Kendrick and Killick-Kendrick, 1999) [* = proven vector, see Killick-Kendrick, 1990a; 1999b]

For detailed distribution ofLeishmaniatransmission by sand flies see underLeishmaniosis.

In general,Ph. ariasi(Rioux et al., 1984) andPh. perniciosus(Izri et al., 1990) were demonstrated as vectors of visceral leishmaniosis and cutaneous leishmaniosis due toL. infantum, both fromPortugaltoItaly and fromMorocco to Tunisia(Rispail et al., 2002).Ph. perfiliewiis proven vector inAlgeria(Izri and Belazzoug, 1993). It is scarce in theSouth East of France(Izri et al., 1994) and more abundant on theAdriatic coast in Italy(Corradetti, 1960).

New World

Lutzomyiais the main genus in the neotropical region, mainly living in the extensive forests of that part of the world.

Distribution of phlebotomines as vectors of Leishmania in the New World

Soon there will be general information on this subject.

References

Corradetti, A.: I focolai italiani di kala azar e il problema della leishmaniosi nel Sud Europa. Parassitologia 2, 95-98, 1960

Izri, M.A., and S. Belazzoug:Phlebotomus (Larroussius) perfiliewinaturally infected with dermotropicLeishmania infantumat Tenes, Algeria. Trans. R. Soc. Trop. Med. Hyg 87,399, 1993

Izri, M.A., S. Belazzoug, Y. Boudjebla, J. Dereure, F. Pratlong, A. Delalbre-Belmonte and J.A. Rioux:Leishmania infantumMON-1 isol dePhlebotomus perniciosus, en Kabylie (Algrie). Ann. Parasitol. Hum. Comp. 65, 151-152, 1990

Izri, M.A., P. Marty, P. Fauran, Y. Le Fichoux and J.J. Rousset:Phlebotomus perfiliewiParrot, 1930 (Diptera: Psychodidae) dans le Sud-Est de le France. Parasite 1, 286, 1994

Killick-Kendrick, R.: Phlebotomine vectors of the leishmaniases: a review. Med. Vet. Entomol. 4, 1-24, 1990a

Killick-Kendrick, R.: The biology and control of phlebotomine sand flies. Clin. Dermatol. 17, 279-289, 1999b

Killick-Kendrick, R., and M. Killick-Kendrick: Biology of sand fly vectors of Mediterranean canine leishmaniasis. In: Killick-Kendrick, R. (ed.): Canine leishmaniasis: an update. Proc. Int. Can. Leishm. Forum, Barcelona, Spain, 1999, Intervet Int., Boxmeer, The Netherlands, pp 26-31, 1999

Lewis, D.J.: A taxonomic review of the genusPhlebotomus(Diptera, Psychodidae). Bull. Br. Mus. Nat. His. 45, 121-209, 1982

Naucke, T.J., and B. Pesson: Presence ofPhlebotomus (Transphlebotomus) mascittiiGrassi, 1908 (Diptera: Psychodidae) in Germany. Parasitol. Res. 86, 335-336, 2000

Rispail, P., D. Jacques and D Jarry: Risk zones of human leishmaniasis in the western Mediterranean Basin. Correlations between vector sand flies, bioclimatology and physiology. Mem. Inst. Oswaldo Cruz 97, 477-483, 2002

Rioux, J.A., D.M. Jarry, G. Lanotte, R. Maazoun and R. Killick-Kendrick: Ecologie des leishmanioses dans le sud de la France. 18. Identification enzymatique deLeishmania infantumNicolle, 1908, isol dePhlebotomus ariasiTonnoir, 1921 spontanment infest en Cvennes. Ann. Parasitol. Hum. Comp. 59, 331-333, 1984

Rioux, J.-A., N. Lger, N. Haddad, M. Gramiccia, L. Jalouk, J. Dereure, A. Al-Khiami and P. Desjeux: Infestation naturelle dePhlebotomus tobbi(Diptera, Psychodidae) parLeishmania donovanis.st. (Kinetoplastida, Trypanosomatidae), en Syrie. Parassitologia 40 (Suppl.), 148, 1998

Old World

Veterinary and Medical ImportanceOverview

Veterinary and medical importance of sand flies is mainly determined by their capability of disease transmission.The following disease hasbeen reported to be transmitted by sand flies:

Leishmaniosis,Leishmania infantum

For detailed information on this subject see underLeishmaniosis

General MorphologySand flies are small insects. Their length, including in females the head, thorax and abdomen and in males the coxites, is 1.2-3.7 mm (Perfil'ev, 1968).Head, thorax, abdomen and appendages are covered with hairs which give a "fluffy" appearance. The palps reach beyond the proboscis and are almost folded in two. The wings are raised above the body. The apex of the wings is directed posteriad and laterad. Legs are long and slender (Perfil'ev, 1968).

Sand flies which are disturbed on a wall do not usually fly, but jump away, rising to the ceiling. This jumping behaviour, the raised wings and the "fluffiness" are reported to be so characteristic that recognition of a live sand fly and distinguishing it from other small insects is possible (Perfil'ev, 1968).

In addition to hairs, sand flies possess scales which are only visible under the microcope. Neither form nor arrangement of both of them are of systematic importance (Perfil'ev, 1968).

Wing venation is subdued to consequent terminology and used as morphological characteristic. Furthermore the anatomy of the head, the structure of the male genitalia, the presence and arrangement of teeth in the cibarium and partly the structure of the female spermathecae is used as characters for the subdivision of genera and subgenera (Peters, 1992).

References

Perfil'ev, P.P.: Fauna of U.S.S.R. Diptera.Phlebotomidae(sandflies). Acad. Sci. U.S.S.R. Zool. Inst. New Ser. No. 93, Vol. 3 No. 2, Israel Program for Scientific Translations, Jerusalem, 1968Peters, W.: Leishmaniases. In: Peters, W. (ed.): A colour atlas of arthropods in clinical medicine. Wolfe Publish. Ltd., London, pp 115-134, 1992

General MorphologyBACKGenera and Species IdentificationGenera and species identification can be performed by standard entomological aspects based on anatomy. Further and newer techniques include biochemical techniques such as enzyme electrophoresis and gas chromatography, DNA probes and monoclonal antibodies.

Standard entomological techniques

Females and males can be distinguished by the naked eye. In females, the end of the abdomen appears blunt. The abdomen is narrow immediately after hatching, inflated and reddish after the first blood meal, brown to black after digestion and markedly thicker with a yellowish shade during egg development. The male abdomen resembles that of unfed females or even thinner and ends in paired appendages, appearing like small spines to the naked eye (Perfil'ev, 1968).

In general, the identification of sand flies is based to a large extent on anatomy. Females of the genera Phlebotomus and Sergentomyia and males of the genus Sergentomyia are identified by anatomical characters. Identification of males of the genus Phlebotomus is based on the morphology of the terminalia (Perfil'ev, 1968).

For further details on anatomy see Perfil'ev, (1968). New techniques (see below) are being introduced to resolve problems of identification, especially when epidemiologically significant females cannot be differentiated (WHO, 1990).

Isoenzyme electrophoresis

A technique used successfully to distinguish species in the Old and the New World. Principal enzymes that vary within and between species are glucose phosphate isomerase, hexokinase, malate dehydrogenase NAD+, malate dehydrogenase NADP+ and phosphoglucomutase (WHO, 1990).

Gas chromatography

It is used for the examination of cuticular hydrcarbon extracts (cuticular lipids Peters, 1992) and has proved to be very useful to distinguish species in which the females were inseparable. It has also been used to highlight geographic variation in other species (WHO, 1990).

DNA probes

Highly specific DNA probes have been developed and offer an ideal tool in epidemiological studies. Sand flies are squashed onto special membranes and sequentially hybridised with probes against the suspected vector and parasite species.

Monoclonal antibodies

They as well are used for identification of sand flies.

References

Perfil'ev, P.P.: Fauna of U.S.S.R. Diptera.Phlebotomidae(sandflies). Acad. Sci. U.S.S.R. Zool. Inst. New Ser. No. 93, Vol. 3 No. 2, Israel Program for Scientific Translations, Jerusalem, 1968WHO: Control of the leishmaniases. Report of a WHO Expert Committee, Tech. Rep. Ser. No. 793, WHO, Geneva, 1990

Sensory OrgansThe ascoid sensillum on the antennae of sand flies has been under examination for electrophysiological response to insect pheromones and kairomones (e.g. Dougherty et al., 1999 for the latter). Specific neurones in ascoid sensilla have been shown to respond to carboxylic acids, ketones, alcohols and aldehydes, components of 'attractive' fox odour.

References

Dougherty, M.J., P.M. Guerin, R.D. Ward and J.G.C. Hamilton: Behavioural and electrophysiological responses of the phlebotomine sandflyLutzomyia longipalpis(Diptera: Psychodidae) when exposed to canid host odour kairomones. Physiol. Entomol. 24, 251-262, 1999

Seasonal and Circadian DynamicsOverview

In temperate climates, in detail the seasonal activity will include the season from April to October in the Old World. Whereas in tropical and neotropical climates, sand fly activity is registered the whole year.

The circadian activity of the adult fly is crepuscular and nocturnal. Many species bite most actively immediately after sunset, but others have been observed to bite after midnight. But this time peak is not universal. It is probable that the fall in temperature and the rise in humidity as the sun goes down are the triggers for this activity.

Depending on the area, and especially the time one hour before until one hour after sunset is the main feeding time. Noli (1999) is extending this time period of activity over the whole night. During day cool and humid resting places are sought (Killick-Kendrick and Killick-Kendrick, 1999).

Numerous studies have been concentrating on daily as well as seasonal activity of phlebotomines. Different methods of collection and different time and place have been practiced.Variations in adult emergence and remaining over the season are according to differences between years and climate, notably temperature at varying altitudes. For the seasonal activity, between one and two peaks of population can be observed in phlebotomines.Taking into account that various phlebotomine species have been classified as reported and suggested vectors of leishmaniosis, seasonal activity and thus risk of transmission stretches between spring and autumn.Generally, depending on the area, temperature, humidity and diverse other environmental factors, sand fly activity can vary to a great extent and thus making general considerations in times very difficult.

References

Killick-Kendrick, R., and M. Killick-Kendrick: Biology of sand fly vectors of Mediterranean canine leishmaniasis. In: Killick-Kendrick, R. (ed.): Canine leishmaniasis: an update. Proc. Int. Can. Leishm. Forum, Barcelona, Spain, 1999, Intervet Int., Boxmeer, The Netherlands, pp 26-31, 1999Noli, C.: Leishmaniose des Hundes. Waltham Focus 9, 16-24, 1999

Old WorldCircadian activity

Italy, Emilia Romagna:In studies,Ph. perfiliewihad its maximum biting activity around 3:00 hours in the morning (Killick-Kendrick et al., 1977).

Iran:A not exclusively nocturnal behaviour inPh. papatasiwas observed, with sand flies still quite active in darkened rooms or shaded animal shelters between 6:30 and 10:00 hours (Javadian et al., 1977).

Oman:The circadian activity of Arabian sand flies, mainlyPh. alexandriandSergentomyia clydei, increased rapidly after sunset (18:50 hours) and was fairly constant on a high level during 9 hours of darkness until dawn, when it decreased rapidly. Few flies were still active at 7:00 hours, 1.5 hours after sunrise. The main factor affecting sandfly activity was light intensity, followed by low relative humidity, followed by low wind velocity. Optimum humidity was around 10%, probable maximum wind velocity was 3.5 m/sec and 11C was the probable minimum temperature. Best nights for catches had a low humidity (10-25%) and low wind speed (< 0.3 m/sec) in combination with highest temperatures (31-43C) (Roberts, 1994).

Seasonal activity

Exemplary, the data of the following regions is listed:

Spain, northeast (Aragon):One of the prevalent sandfly species,Sergentomyia minuta, which is also prevalent in diverse other localities of the Mediterranean Area (see Benito-De Martin et al., 1991), reached its highest density in the coldest and most humid areas of the Northeast of Spain. Seasonal activity in the was depending on the degree of urbanization with the longest span (6 months) in suburban areas, decreasing towards periurban and rural foci. The species showed one (July-August) as well as two (June, August-September) peaks of density depending on the area and vegetation (Benito-De Martin et al., 1991).

Spain,south:The longest seasonal activity period recorded in this area has been nine months (Martinez-Ortega, 1984; Morillas-Marquez et al., 1983; Sanchis-Marin et al., 1986).

Jordan, southern Jordan Valley:The most abundant sandfly,Ph. papatasi, which distribution and temporal association points to significance in the transmission ofLeishmania, had its peak abundance in September and October, then declining sharply by late November (Janini et al. 1995).

Kenya:Sandfly population was highest during the rainy seasons, April-June and November-December. A significant association was observed between monthly sandfly abundance and rainfall in the previous month (Robert et al., 1994).

Senegal:The three most abundant species of the study,S. dubia,S. schwetzi,S. buxtoni, had their population peak in February (Ba et al., 1998).

India:Ph. papatasishowed its maximum indoor resting density during the monsoon season. A positive correlation between density and rainfall could be observed. The finite rate of natural increase of the field population was maximum in October and minimum in April (Srinivasan et al. 1993), similar to findings on the African continent.

References

Ba, Y., J. Trouillet, J. Thonnon and D. Fontenille:Phlbotomes du Sngal (Diptera Psychodidae): peuplement et dynamique des populations de la region de Mont-Rolland. Parasite 5, 143-150, 1998

Benito-De Martin, M.I., J. Lucientes-Curdi, J. Orcajo-Teresa and J.A. Castillo-Hernandez: Seasonal dynamics ofSergentomyia minuta(Rondani, 1843) populations in Aragon (N. E. Spain). Parassitologia 33 (Suppl.) 89-97, 1991

Janini, R., E. Saliba and S. Kamhawi: Species composition of sand flies and population dynamics ofPhlebotomus papatasi(Diptera: Psychodidae) in the southern Jordan Valley, an endemic focus of cutaneous leishmaniasis. J. Med. Entomol. 32, 822-826, 1995

Javadian, E., R. Tesh, S. Saidi and A. Nadim: Studies on the epidemiology of sandfly fever in Iran III. Host-feeding patterns ofPhlebotomus papatasiin an endemic area of the disease. Am. J. Trop. Med. Hyg. 26, 294-298, 1977

Killick-Kendrick, R., P.D. Ready and S. Pampiglione: Notes on the prevalence and host preferences ofPhlebotomus perfiliewiin Emilia-Romagna, Italy. In: Rioux, J.-A. (ed.): Ecologie des Leishmanioses. Coll. Internat. CNRS No. 239, Montpellier, France, 1974, pp 169-175, 1977

Martinez-Ortega, E.: Fenologa deSergentomyia minuta(Rondani, 1843) (Diptera, Psychodidae, Phlebotominae) en el sureste de la Peninsula Ibrica. Bol. Asoc. Esp. Entomol. 8, 35-39, 1984

Morillas-Marquez, F., D.C. Guevara-Benitez, J. M. Ubeda-Ontiveros and J. Gonzalez-Castro: Fluctuations annuelles des populations de Phlbotomes (Diptera, Phlebotomidae) dans la province de Grenade (Espagne). Ann. Parasitol. Hum. Comp. 58, 625-632, 1983

Robert, L.L., K.U. Schaefer, and R.N. Johnson: Phlebotomine sandflies associated with households of human visceral leishmaniasis cases in Baringo District, Kenya. 88, 649-657, 1994

Roberts, D.M.: Arabian sandflies (Diptera: Psychodidae) prefer the hottest nights? Med. Vet. Entomol. 8, 194-198, 1994

Sanchis-Marin, M., F. Morillas-Marquez, J. Gonzalez-Castro, I. Benavides-Delgado and A. Reyes-Magaa: Dinmica estacional de los flebotomos (Diptera, Phlebotomidae) de la provincia de Almeria (Espaa). Rev. Iber. Parasitol. 46, 285-291, 1986

Srinivasan, R., K.N. Panicker and V. Dhanda: Population dynamics ofPhlebotomus papatasi(Diptera: Phlebotomidae) in Pondicherry, India. Acta Trop. 54, 125-130, 1993

New WorldCircadian activity

Mexico:Maximum bite rate ofLu. cruciatain was found between 18:00 and 19:00 hours. Host-seeking females were observed to be directly related to levels of humidity (Rebollar-Tellez et al., 1996).

Colombia:Field studies withLu. longipalpisrevealed increased activity shortly after sunset, continuing until just after sunrise. Furthermore peak sandfly activity was greatest early in the evening (18:30-23:30 hours) and then declined steadily towards morning (Morrison et al., 1995b).

Venezuela, Caribbean coast:ObservingLu. evansiandLu. panamensis, maximum landing / biting activity ofLu. evansiwas observed at 24:00 and 3:00 hours. ForLu. panamensismaximum landing/biting activity was observed between 2:00 and 03:00 hours (Gonzlez et al., 1999).

Seasonal activity

Mexico:Population dynamic studies revealed highest peak population forLu. cruciatain March, and lesser peaks in February, December and January of the study years (Rebollar-Tellez et al., 1996).

Venezuela:Lu. evansiwas most abundant in October and July, associated with a bimodal cycle of annual rainfall in the area.Lu. panamensisshowed maximal landing / biting activity in June, slightly preceding the annual rainfall maximum in July, and a secondary peak in December, somewhat after the secondary rainfall maximum in October, coinciding with the start of the December-February dry season (Gonzlez et al., 1999).In the northern part of the country further seasonal activity ofLu. panamensiswas reported by (Feliciangeli, 1987). In their studies the species behaved as a wetseason species with mean minimum relative humidity as critical factor influencing the total number of individuals. Decreasing population numbers were replaced byLu. ovallesi, a dry-season species.

Colombia:A bimodal annual abundance cycle with a small peak in October-November and a larger peak in April-May (prominent 6-mo cycle) was observed forLu. longipalpis(Morrison et al., 1995a).In studies in the northern part of the country,Lu. evansi, the vector of visceral leishmaniosis, was predominant. Generally the sand flies were present throughout the year with exception of the driest months (February and March). Parous and infected sand flies were most abundant towards the end of the rainy season (October-December) (Travi et al. 1996).

USA, Texas:Lu. diabolicahad its peak abundance in July in Texas (McHugh et al., 2001).

USA, Georgia:The first appearanceLu. shannoni, was recorded in April. Peaks of abundance followed in May (the one year) and May and July (the following year), again followed by rapid reduction in October and November respectively September and October. No specimens were collected in December respectively March, November and December (Brinson et al., 1992).

References

Brinson, F.J., D.V. Hagan, J.A. Comer and D.A. Strohlein: Seasonal abundance ofLutzomyia shannoni(Diptera: Psychodidae) on Ossabaw Island, Georgia. J. Med. Entomol. 29, 178-182, 1992

Feliciangeli, M.D.: Ecology of sandflies (Diptera: Psychodidae) in a restricted focus of cutaneous leishmaniasis in northern Venezuela. III. Seasonal fluctuation. Mem. Inst. Oswaldo Cruz 82, 167-176, 1987

Gonzlez, R., L. De Sousa, R. Devera, A. Jorquera, and E. Ledezma: Seasonal and nocturnal human landing/biting behaviour ofLutzomyia(Lutzomyia)evansiandLutzomyia(Psychdopygus)panamensis(Diptera: Psychodidae) in a periurban area of a city on the Caribbean coats of eastern Venezuela (Barcelona; Anzotegui State). Trans. R. Soc. Trop. Med. Hyg. 93, 361-364, 1999

McHugh, C.P., B.F. Ostrander, R.W. Raymond, and S.F. Kerr: Population dynamics of sand flies (Diptera: Psychodidae) at two foci of leishmaniasis in Texas. J. Med. Entomol. 38, 268-277, 2001

Morrison, A.C., C. Ferro, R. Pardo, M. Torres, B. Devlin, M.L. Wilson and R.B. Tesh: Seasonal abundance ofLutzomyia longipalpis(Diptera: Psychodidae) at an endemic focus of visceral leishmaniasis in Colombia. J. Med. Entomol. 32, 538-548, 1995a

Morrison, A.C., C. Ferro, R. Pardo, M. Torres, M.L. Wilson, and R.B. Tesh: Nocturnal activity patterns ofLutzomyia longipalpis(Diptera: Psychodidae) at an endemic focus of visceral leishmaniasis in Colombia. J. Med. Entomol. 32, 605-617, 1995b

Rebollar-Tellez, E.A., F. Reyes-Villanueva, I. Fernandez-Salas, and F.J. Andrade-Narvaez: Population dynamics and biting rhythm of the anthropophilic sandflyLutzomyia cruciata(Diptera: Psychodidae) in Southeast, Mexico. Rev. Inst. Med. Trop. So Paulo 38, 29-33, 1996

Travi, B.L., J. Montoya, J. Gallego, C. Jaramillo, R. Llano and I.D. Velez: Bionomics ofLutzomyia evansi(Diptera: Psychodidae) vector of visceral leishmaniasis in northern Columbia. J. Med. Entomol. 33, 278-285, 1996

Host Seeking BehaviourIn contrast to mosquitoes (and tsetse flies) only minimal data exists in the field of sand fly attraction to the host. Research into olfactory responses of bloodsucking insects to host odours is contributing to a better understanding of vector behaviour, as well as to the identification of more effective trapping methods for monitoring or control purposes. For further reading see e.g. Gibson and Torr (1999).

In the field of host seeking behaviour in sand flies, measurements of host preference or anthrophily have mainly been performed by the identification of bloodmeal origin from wild caught female sand flies or the use of human and animal baits (e.g. Christensen and Herrer, 1980; Quinnell et al., 1992; Montoya-Lerma and Lane, 1996; Campbell-Lendrum et al., 1999). But bloodmeal data has according to Pinto et al. (2001) to be interpreted with caution as they reflect not only innate vector preferences, but also the relative abundance and accessibility of host species in the local environment. For a more obvious judgement of the preferences reflected by different bloodmeals the forage ratio and the host selectivity index have been designed.

Generally adult phlebotomines reportedly exhibit specific activity periods for events such as host-seeking, sugar- and blood-feeding, mating, and oviposition. Flight activity is triggered by daily changes in light intensity (Chaniotis et al., 1971) and further modified by other abiotic factors such as temperature, relative humidity, cloud cover, rain, and wind velocity (Hoogstraal et al., 1962; Quate, 1964). Most phlebotomine sand flies are crepuscular and nocturnal biters (Chaniotis et al., 1971). Feeding, however, is discontinuous and sporadic within the course of a single evening (Rosabal and Trejos, 1965; Chaniotis et al., 1971). For further information see 'Circadian and seasonal activity'.

Direct evidence for odour-mediated host preferences results from studies on different attraction to a range of animal baits in the field (Christensen and Herrer, 1973; Quinnell et al., 1992; Montoya-Lerma and Lane, 1996; Campbell-Lendrum et al., 1999), or to extracted volatiles of different hosts in the laboratory (Hamilton and Ramsoondar, 1994; Rebollar-Tellez et al., 1999).

Feeding Habits

Diverse feeding habits are distinguished in haematophageous insects:

anthropophagic / anthropophilic: sand flies biting (preferably) humans zoophagic / zoophilic: sand flies biting lifestock and other animals endophagic: sand flies biting mainly inside houses endophilic: sand flies resting indoors after blood-feeding while the meal is digested and the eggs mature exophagic: sand flies biting mainly out of doors exophilic: sand flies resting outdoors after blood-feeding while the meal is digested and the eggs mature

CO2

Sand flies being attracted to a range of hosts must be responsive to ubiquitous host odour cues such as CO2(Pinto et al., 2001). This explains why the rate of attraction seems to increase with host size in many sandfly species (Quinnell et al., 1992; Campbell-Lendrum et al., 1999), while this is still debatable (e.g. Christensen and Herrer, 1980).

Generally, haematophagous insects are attracted by CO2concentration gradients, and the attractiveness of other host odours is synergized by CO2(Nicolas and Sillans, 1989; Mboera and Takken, 1997; Gibson and Torr, 1999). In the field CO2from dry ice has proven to be an attractant for sand flies (first indicated by Knudsen et al. (1979)), but not always shown effective in laboratory assays (Nigam and Ward, 1991). Using so-called odour-baited entry traps (OBETs) (Costatini et al., 1993), working along the principle to isolate the tested odour from other cues as vision, temperature and humidity, and to generate wind flow carrying odours to exploit anemotaxis behaviour (of flying insects), Pinto et al. (2001) could prove that anthropophilic sand flies (Lu. intermediaandLu. whitmani) were attracted by human kairomones in addition to CO2. The role of the single odours respectively CO2varied with sandfly gender (Pinto et al., 2001).

Other Host Odour Compounds

Information on host odours apart from CO2in sand flies is minimal. Octenol, a well known cattle-derived attractant for tsetse flies has not proven to increase attractivity inPh. argentipesin traps in field studies (Cameron et al., 1991).

Human skin odour deposited on a rubbed petri dish did show various attraction toLu. longipalpis(Hamilton and Ramsoondar, 1994). Even transfer of volatiles responsible for attraction to new petri dishes after extraction has been successfully performed (Rebollar-Tellez et al., 1999). None of these studies identified single components or provided information on the chemical constituents of the kairomones. Whereas Dougherty et al. (1999) managed to create a synthetic mix of compounds mimicking fox odour and being comparable attractive. And even though the single compounds did not induce the same response as whole fox odour, benzaldehyde, 4-hydroxy-4-methyl-2-pentanone and methyl-2-pentanone attracted sand flies in wind-tunnel choice experiments.

Sandfly Pheromones

Sandfly pheromones have also been proven to be attractive. Ward (1986) showed a significant increase in host attractivity to female flies when in the presence ofLu. longipalpismales. Hamilton et al. (1994) demonstrated pheromone fractions which were responsible for female sand fly attraction.Pinto et al. (2001) suggest the initial arrival of male sand flies on a host as response to attractive odour cues, but male aggregations on hosts as presumably mediated by sandfly pheromones (Dye et al., 1991).

In the genusPhlebotomusno chemical or biological evidence for pheromones has so far been given.

References

Cameron, M.M., F.P. Amerisinghe and R.P. Lane: The field response of Sri Lanka sandflies and mosquitoes to synthetic cattle-derived attractants. Parassitologia 33, 119-126, 1991

Campbell-Lendrum, D.H., M.C. Pinto, S.P. Brando-Filho, A.A. de Souza, P.D. Ready and C.R. Davies: Experimental comparison of anthropophily between geographically dispersed populations ofLutzomyia whitmani(Diptera Psychodidae). Med. Vet. Entomol. 13, 299-309, 1999

Chaniotis, B.N., M.A. Correa, R.B. Tesh and K.M. Johnson: Daily and seasonal man-biting activity of phlebotomine sandflies in Panama. J. Med. Entomol. 8, 415-420, 1971

Christensen, H.A., and A. Herrer: PanamanianLutzomyia(Diptera: Psychodidae) host attraction profiles. J. Med. Entomol. 17, 522-528, 1980

Costatini, C., G. Gibson, J. Brady, L. Merzagora and M. Coluzzi: A new odour-baited trap to collect host seeking mosquitoes. Parassitologia 35, 5-9, 1993

Dougherty, M.J., P.M. Guerin, R.D. Ward and J.G.C. Hamilton: Behavioural and electrophysiological responses of the phlebotomine sandflyLutzomyia longipalpis(Diptera: Psychodidae) when exposed to canid host odour kairomones. Physiol. Entomol. 24, 251-262, 1999

Dye, C., C.R. Davies and R. Lainson: Communication among phlebotomine sand flies: a field study of domesticatedLutzomyia longipalpispopulations in Amazonian Brazil. Anim. Behav. 42, 183-192, 1991

Gibson, G., and S.J. Torr: Visual and olfactory responses of haematophagous Diptera to host stimuli. Med. Vet. Entomol. 13, 2-23, 1999

Hamilton, J.G.C., and T.M.C. Ramsoondar: Attraction ofLutzomyia longipalpisto human host odours. Med. Vet. Entomol. 8, 375-380, 1994

Hamilton, J.G.C., M. Dougherty, and R.D. Ward: Sex pheromone activity in a single component of tergal gland extract ofLutzomyia longipalpis(Diptera: Psychodidae) from Jacobina, North Eastern Brazil. J. Chem. Ecol. 20, 141-151, 1994

Hoogstraal, H., D.R. Dietlein and D. Heyneman: Leishmaniasis in the Sudan Republic. 4. Preliminary observations on man-biting sandflies (Psychodidae:Phlebotomus) in certain Upper Nile endemic areas. Trans. R. Soc. Trop. Med. Hyg. 56, 411-422, 1962

Knudsen, A.B., D.J. Lewis, R.B. Tesh, A. Rudnick, J. Jeffery and I. Singh: Phlebotomine sand flies (Diptera: Psychodidae) from a primary hill forest in West Malaysia. J. Med. Entomol. 15, 286-291, 1979

Mboera, L.E.G., and W. Takken: Carbon dioxide chemotropism in mosquitoes (Diptera: Culicidae) and its potential in vector surveillance and management programmes. Rev. Med. Vet. Entomol. 85, 355-368, 1997

Montoya-Lerma, J., and R.P. Lane: Factors affecting host preference ofLutzomyia evansi(Diptera: Psychodidae), a vector of visceral leishmaniasis in Colombia. Bull. Entomol. Res. 86, 43-50, 1996

Nicolas, G., and D. Sillans: Immediate and latent effects of carbon dioxide on insects. Ann. Rev. Entomol. 34, 97-116, 1989

Nigam, Y., and R.D. Ward: The effect of male sand fly pheromone and host factors as attractants for femaleLutzomyia longipalpis(Diptera: Psychodidae). Physiol. Entomol. 16, 305-312, 1991

Pinto, M.C., D.H. Campbell-Lendrum, A.L. Lozovei, U. Teodoro and C.R. Davies: Phlebotomine sandfly responses to carbon dioxide and human odour in the field. Med. Vet. Entomol. 15, 132-139, 2001

Quate, L.W.:Phlebotomussandflies of the Paloich area in the Sudan (Diptera, Psychodidae). J. Med Entomol. 1, 213-268, 1964

Quinnell, R.J., C. Dye and J.J. Shaw: Host preferences of the phlebotomine sandflyLutzomyia longipalpisin Amazonian Brazil. Med. Vet. Entomol. 6, 195-200, 1992

Rebollar-Tellez, E.A., J.G.C. Hamilton and D. Ward: Response of femaleLutzomyia longipalpisto host odour kairomones from human skin. Physiol. Entomol. 24, 220-226, 1999

Rosabal, R., and A. Trejos:Phlebotomusde El Salvador (Diptera: Psychodidae) II. Observaciones sobre su biologa con especial referencia aP. longipalpis. Rev. Biol. Trop. 13, 219-228, 1965

Ward, R.D.: Mate recognition in a sand fly (Diptera: Psychodidae). J. R. Army Med. Corps 132, 312-134, 1986

Host SpectrumSand flies possess a wide spectrum of hosts. The most important hosts are rodents, dogs and man, due to the capacity of being a zoonotic reservoir forLeishmania. Apart from these, domestic livestock, other carnivores, as well as reptiles and amphibia also belong to the host spectrum.

The Indian desert gerbil (Meriones hurrianae), the fat-tailed sand rat (Psammomys obesus), the great gerbil (Rhombomys opimus), the rock hyrax (Procavia capensis) and the bush hyrax (Heterohyrax brucei), the lesser ant-eater (Tamandua teradactyla), the opossum (Didelphis marsupialis) (in Brazil e.g.) and the Panamanian (Choloepus hoffmanni) and the Brazilian two-toed sloth (Choloepus didactylus), to mention only some, belong to the host spectrum of sand flies and have been proven to be important reservoir hosts for different species ofLeishmania.

Developmental CycleThe biology of each species of sand fly is unique and complex, covering all aspects of reproduction, feeding, dispersal and other activities, being of importance for epidemiology of transmitted diseases and vector control (WHO, 1990).

Sand flies undergo complete metamorphosis, passing through four distinct stages during their life cycle: egg, larvae, pupa, adult / imago.

In arid and temperate regions, larvae may remain in a state of diapause for many months. In temperate countries, sand flies over-winter as eggs or larvae in a so-called diapause. For this reason, adults can appear early in summer, and leishmaniosis as one the sand fly-borne diseases can exist in places with a cold winter (Lewis, 1971). Similarly, diapause might also be the means by which many tropical sand flies survive periods of drought or heavy rain (Ward and Killick-Kendrick, 1974).

Palaearctic sand flies over-winter as fourth instar larvae (Killick-Kendrick and Killick-Kendrick, 1987).From laboratory studies, a complete gonotrophic cycle is normally not less than 6 weeks, but can differ between different species (Killick-Kendrick and Killick-Kendrick, 1999).

EggEggs are oblong-oval, minute (average 0.3-0.4 mm according to Shevchenko, 1929) and difficult to find in nature. Newly-laid eggs are soft, light yellow, with a shiny surface. After several hours they darken, become hard, dark brown and show characteristic thin ridges (Perfil'ev, 1968).

They are laid in cracks and crevices in moist ground, among leaf litter, between buttress roots of trees, at the bases of termite mounds, on stable floors and in poultry sheds, where adult flies rest and the microclimate is high.

The site and type of habitat is species-dependent. Between 10/15 and 100 eggs are laid in a single batch (40-70 usually in one oviposition cycle (WHO, 1990)). Under optimum conditions they hatch in 6-17 days. Longer periods are necessary in cooler conditions.

References

Perfil'ev, P.P.: Fauna of U.S.S.R. Diptera.Phlebotomidae(sandflies). Acad. Sci. U.S.S.R. Zool. Inst. New Ser. No. 93, Vol. 3 No. 2, Israel Program for Scientific Translations, Jerusalem, 1968 Shevchenko, F.I.:Vneshnyaya morfologiya lichinok moskitov.P. papatasi,P. chinensis,P. sergenti(The external morphology of sandfly larvae (P. papatasi,P. chinensis,P. sergenti)). Meditsinskaya Mysl' Uzbekistana I Turkmenistana, Nos 7/8, 67-83, 1929-1930WHO: Control of the leishmaniases. Report of a WHO Expert Committee, Tech. Rep. Ser. No. 793, WHO, Geneva, 1990

LarvaThe maggot-like first stage larva can be identified by the presence of one pair of long caudal bristles, which is seen through the egg shell. Following stage larvae are progressively larger than first-stage larvae and possess two pair of caudal bristles. All larval stages show phlebotomine larvae characteristic 'matchstick' hairs on each segment.

Four instars of larvae follow over a period of 21-60 days (Peters, 1992) / 16-90 days (Service, 2001a). Larvae are mainly scavengers. In laboratories, they are fed on semi-rotting vegetable matter and decomposing arthropod bodies, chow or even feces of vertebrates (e.g. aged rabbit faeces (Singh, 1985, based on Endris et al. 1982). The developing larva is cutting an exit hole with a sort of 'egg tooth' into the egg shell.

The final-instar larva sheds its skin and the pupa is formed. Larval breeding sites are seldom found, Bettini and Melis (1988) suggested pre-imaginal stages associated with a comparatively stable, cool, humid environment, protected from rain and sunshine and in the special analyzed site, rich in clay and organic nitrogen.

References

Bettini, S., and P. Melis: Leishmaniasis in Sardinia. III. Soil analysis of a breeding site of three species of sandflies. Med. Vet. Entomol. 2, 67-71, 1988 Endris, R.G., P.V. Perkins, D.G. Young and R.N. Johnson: Techniques for laboratory rearing of sand flies (Diptera: Psychodidae). Mosq. News 42, 400-407, 1982 Peters, W.: Leishmaniases. In: Peters, W. (ed.): A colour atlas of arthropods in clinical medicine. Wolfe Publish. Ltd., London, pp 115-134, 1992 Singh, P.: Multiple-species rearing diets. Diptera: Psychodidae. In: Singh, P., and R. F. Moore (eds.): Handbook of Insect Rearing. Vol. 1 Elsevier, Amsterdam, pp 33-34, 1985Service, M.W.: Phlebotomine sand-flies (Phlebotominae). In: Service, M. W. (ed.): The encyclopedia of arthropod-transmitted infections. CABI Publish., Oxon, New York, pp 395-397, 2001a

PupaThe pupae of sand flies are 3 mm long and club-shaped. The narrow part is curved and head and thorax are curved backwards. The posterior segments are covered with the exuviae of the fourth-stage larva. With it the pupa is attached to the substrate in a usually vertical position (Perfil'ev, 1968). After approximately 5-10 days the adult emerges.

References

Perfil'ev, P.P.: Fauna of U.S.S.R. Diptera.Phlebotomidae(sandflies). Acad. Sci. U.S.S.R. Zool. Inst. New Ser. No. 93, Vol. 3 No. 2, Israel Program for Scientific Translations, Jerusalem, 1968

AdultAdults can be identified from other insects by their behaviour, appearance, size etc. (see there) Both sexes feed on plant sugars (Lewis and Domoney, 1966). Killick-Kendrick (1979) also describes honeydew of aphids and coccids as possible source.

In studies (Chaniotis, 1974) it as been shown that some sugars are preferred to others which could mean that preferences for particular plants may restrict the distribution of the insect and thus also of possible transmissible parasites. The type of sugar and the frequency of uptake may be a factor in the insect's ability to transmit leishmaniosis. Plant sugars may be essential for parasite survival and promastigotes require carbohydrates for their development (Killick-Kendrick, 1978).

Only females feed on blood, which is suspected as a source of protein for egg development. When seeking food sand flies normally have a characteristic short hopping flight.

Females require the blood meal to mature about 80-100 eggs and the time from engorgement to oviposition is not less than 6 days (demonstrated in Mediterranean species) (Killick-Kendrick and Killick-Kendrick, 1999). Males are attracted to females when those are feeding and will mate with them even while the females are taking a blood meal. Mating behavior of sand flies differs between species, with some males arriving on the host before the female, courting the females when they come to feed (Jarvis and Rutledge, 1992; Lane et al., 1990). Others ride on the back of the female before copulation (Valenta et al., 2000), whereas Ph. ariasi is suggested to mate after the females have fed (Killick- Kendrick and Killick-Kendrick, 1999).

Life Expectancy

Life expectancy has hardly been determined for wild female sand flies. Killick-Kendrick et al. (1984) recaptured markedPh. ariasi28 days after release.

Autogeny

Autogeny i.e. the ability to produce eggs without a bloodmeal has been reported for some sand fly species (Johnson, 1961; Schmidt, 1965) and suspected for others (Lewis et al., 1970). But it is less common than in mosquitoes (Killick-Kendrick, 1978). Autogeny may help a sand fly population to increase quickly. Thus bring a rapid onset of the maximum Leishmania transmission period (Lewis, 1971). While it has not been demonstrated for the Mediterranean vectors (Killick-Kendrick and Killick-Kendrick, 1999).In nature, more than one gonotrophic cycle is considered normal (Dolmatova, 1942), whereas in the laboratory, most gravid females lay eggs and die either as they lay or shortly afterwards.

For some subgenera ofPhlebotomusthe females are gonotrophically concordant and take one blood meal each gonotrophic cycle (Killick-Kendrick and Killick-Kendrick, 1999).

MostLeishmaniaspecies complete their life-cycle within a single ovarian cycle of the sand fly, and parasites may therefore be transmitted at the first bloodmeal after an infective feed. But in some (L. d. donovaniand some strains ofL. d. infantum) the development is not complete until after the second bloodmeal. This means full life cycles cannot be demonstrated under laboratory conditions when sand flies do not survive oviposition (Killick-Kendrick, 1978).

References

Chaniotis, B.N.: Sugar-feeding behavior ofLutzomyia trapidoi(Diptera: Psychodidae) under experimental conditions. J. Med. Ent. 11, 73-79, 1974 Dolmatova, A.V.: Life cycle ofPhlebotomus papatasi(Scopoli). (in Russian) Med. Parazit. (Mosk.) 11, 32-70, 1942 Jarvis, E.K., and L.C. Rutledge: Laboratory observations on mating and leklike aggregations inLutzomyia longipalpis(Diptera: Psychodidae). J. Med. Entomol. 29, 171-177 aus Killick-Kendrick Barcelona S. 26 ff, 1992 Johnson, P.T.: Autogeny in PanamanianPhlebotomussandflies. Ann. Ent. Soc. Amer. 54, 116-118, 1961 Killick-Kendrick, R.: Recent advances and outstanding problems in the biology of phlebotomine sandflies. Acta Trop. 35, 297-313, 1978 Killick-Kendrick, R.: Biology ofLeishmaniain phlebotomine sandflies. In: Lumsden, W.H.R., and D.A. Evans (eds.): Biology of the Kinetoplastida. Vol. 2, Academic Press, London, New York, pp 395-460, 1979 Killick-Kendrick, R., and M. Killick-Kendrick: Biology of sand fly vectors of Mediterranean canine leishmaniosis. In: Killick-Kendrick, R. (ed.): Canine leishmaniasis: an update. Proc. Int. Can. Leishm. Forum, Barcelona, Spain, 1999, Intervet Int., Boxmeer, The Netherlands, pp 26-31, 1999 Killick-Kendrick, R., J.-A. Rioux, M. Bailly, M.W. Guy, T.J. Wilkes, F.M. Guy, I. Davidson, R. Knechtli, R.D. Ward, E. Guilvard, J. Prires and H. Dubois: Ecology of leishmaniasis in the south of France. 20. Dispersal ofPhlebotomus ariasiTonnoir, 1921 as a factor in the spread of visceral leishmaniasis in the Cvennes. Ann. Parasitol. Hum. Comp. 59, 555-572, 1984 Lane, R.P., M.M. Pile and F.P. Amerasinghe: Anthropophagy and aggregation behaviour of the sandflyPhlebotomus argentipesin Sri Lanka. Med. Vet. Entomol. 4, 79-88, 1990 Lewis, D.J., and C.R. Domoney: Sugar meals in Phlebotominae and Simuliidae. Proc. R. Ent. Soc. Lond. A 41, 175-179, 1966 Lewis, D.J., R. Lainson and J.J. Shaw: Determination of parous rates in Phlebotomine sandflies with special reference to Amazonian species. Bull. Ent. Res. 60, 209-219, 1970 Lewis, D.J.: Phlebotomid sandflies. Bull. WHO 44, 535-551, 1971 Schmidt, M.L.: Autogenic development ofPhlebotomus papatasi(Scopoli) from Egypt. J. Med. Ent. 1, 356, 1965 Valenta, D.T., R. Killick-Kendrick and M. Killick-Kendrick: Courtship and mating by the sandflyPhlebotomus duboscqi, a vector of zoonotic cutaneous leishmaniosis in the Afrotropical region. Med. Vet. Entomol. 14, 207-212, 2000

ControlBest protection may be provided by regular use of anti-parasite products with a repellent action.