Sandfly diet and Leishmania

Abstract

The diet of female phlebotomine sandflies is made up of regular sugar meals and the infrequent blood meals which induce oogenesis. Thus the environment for Leishmania development in the gut com- prises two different nutrient media and their respective digestive enzymes. Amas- tigote forms of the parasr~e are ingested with the blood meal which is gradually digested and is followed by sugar meals. During this time the amastigotes transform into various flagellated forms, including the infective forms which move forward into the proboscis to be transmitted to a new host when another blood meal is taken L2. Very little is known about the effect of sandfly diet or gut enzymes on the development of Leishmania. But there is evidence that establishment of infection in the gut and transmission by bite, both essential for the perpetuation of the para~ sites, depend on components of the sandfly meal. Blood Meal and Vector Specificity Each vector of Old World Leishmania tends to transmit only one species of the paras~e. In contrast, New World vectors can support infections of various Leishmania species. The selectivity of Old World vectors was shown by artificial membrane feeding of Phlebotomus papatasi with meals that contained a small number of parasites in 50% rabbit serum 3. The susceptibility to infection with parasite strains not normally transmitted by this sandfly increased considerably when the flies ingested a large number of promasti- gates or when the meals were made up of 10% serum or saline. This suggests that under natural conditions the non-transmit- ted strains of Leishmania are destroyed by products of serum digestion 3. In the sandfly gut, levels of proteases rise after the ingestion of blood 4, and these enzymes could be the effectors of Leishmania selection. We compared the effects of the naturally transmitted L. major and of L. donovani (introduced artificially by membrane feeding) on the gut enzymes of P. papotasi; substrate digestion by gut preparations of flies harbouring L. major was a third less, and of similar preparations of L. donovani a third greater, than that of uninfected controls. But pro- mastJgotes of both Leishmania species enhanced the proteolytic activrty when added in vitro to control gut preparations (Y. Schlein and H. Romano, unpublished), This enhancement of activity is the direct effect of the parasites on the enzymes, so the decrease caused in vivo by L. major seems to result from inhibition of enzyme production. L. donovani, which is not adapted to this vector, seems unable to inhibit the production of gut enzymes, Other evidence for the apparent role of enzymes in vector competence is the death of L. major in P. papatasi fed on turkey blood before or after the infective meal. In this case the measured DNAase level induced bythe avian blood was much higher than that measured following rabbit blood meals 5. These observations suggest that Leishmania can tolerate only a certain level of some enzymes in the gut. This level varies according to the source of the blood meal and could thereby render the vector unsuitable for harbouring the Leishmania it transmits in nature. The indiscriminate viability of Leish- mania in the New World vectors is a trait of the sandflies. L major (= k tropica) from Israel, which is normally transmitted by P. papatasi in the Old World, can also infect the New World vectors Lutzomyia Iongipalpis and Lu. renei 6. On the basis of their behaviour in the vector, mammalian species of Leishmania have been classified in two groups: the peripylaria which multiply in the hindgut, and suprapylaria which develop only anterior to the hindgut The peripylaria includes the L braziliensis complex, and the suprapylaria comprises other neo- tropical and Old World species 7. How- ever, suprapylarians can change their location. This is shown by studies of the