Host Preferences of the Phiebotomine Sandfly Lutzomyia Longipalpis in Amazonian Brazil
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Medicai and Veterinary Eníomology (1992) 6, 195-2(K) Host preferences of the phiebotomine sandfly Lutzomyia longipalpis in Amazonian Brazil R. J. QUINNELL, C. DYE and J. J. SHAW* Department of Medicai Parasitology, London School of Hygiene and Tropical Medicine, and *Wellconie Parasitology Unií, Instituto Evandro Chagas, CP. 3, Belém, 66001 Pará, Brazil Abstract. Experiments were undertaken to determine the relative attractiveness of humans, dogs and chickens to Lutzomyia longipalpis, the principal vector of Leishmania chagasi causing American visceral leishmaniasis. Field experiments in two villages on Marajó Island, Pará State, Brazil, showed that one boy at- tracted significantly more flies than one dog or chicken, and slightly fewer flies than a group of six chickens. Experiments with laboratory-bred female flies showed that a significantly greater number of flies engorged on a single human than on either a single dog or chicken, and man-biting catches demonstrated the willingness of flies to bite in the field. It appears that Lu.longipalpis has catholic feeding habits, the attractiveness of different hosts being largely a function of their relative sizes. These results are discussed with reference to the epidemiology of visceral leishmaniasis in Brazil. Key words. Lutzomyia longipalpis, Phlebotominae, sandfly, host preference, visceral leishmaniasis, Leishmania chagasi, Amazónia, Brazil. Introduction also been found in smaller numbers in some forest áreas (Lainson et al., 1990). Despite its abundance, very little is The phiebotomine sandfly Lutzomyia longipalpis Lutz known of its innate host preferences or its actual biting be- & Neiva (Diptera: Psychodidae) is the most important haviour. In northeast Brazil, e.g. Ceará State, Lu.longi• vector of American visceral leishmaniasis (AVL), caused palpis is considered to be anthropophilic, readily biting by Leishmania chagasi Cunha & Chagas (Lainson et ah, man (Deane & Deane, 1962; Ward et al., 1983). Deane 1977; Lewis & Ward, 1987). In most áreas it is the only (1956) captured more flies on people than on dogs, although known vector, although Lu.evansi is an alternate vector in the largest numbers were caught on donkeys, and up to Colômbia (Travi et al., 1990). 2608 Lu.longipalpis females have been captured inside a Although AVL occurs from México to Argentina single house (Deane & Deane, 1962). In Costa Rica, (Grimaldi et al., 1989), over 90% of human cases come Zeledon et al. (1984) captured similar numbers of flies from Brazil. Within Brazil there are large regional dif- on people, dogs, pigs, horses and cattle. By contrast, ferences: of 9295 cases reported during 1983-88, 8740 in Amazonian Brazil, casual observations suggest "that were from the northeast and only 193 from the Amazon Lu.longipalpis is 'not particularly anthropophilic, and region (Vieira et al., 1990). AVL is thought to be largely much more inclined to feed on dogs' (Lainson & Shaw, zoonotic, the most important reservoir hosts being the 1979). In Rio de Janiero State, Aguiar e/a/. (1987) captured domestic dog and various wiid canids, especially Cerdocyon more flies on chickens than either people or dogs. Corredor thous (L.) (Deane, 1956; Lainson etal., 1990). Prevalence et al. (1989) made night biting collections in Colômbia and of infection is generally greater in dogs than in humans 'observed repeatedly that [Lu.longipalpis] prefer to feed (Deane, 1961), although few surveyshave used comparable on domestic animais, including poultry, if these animais techniques in both populations. are available.' In Brazil Lu.longipalpis is often abundant peridomesti- None of these studies amount to definitive field exper• cally, especially in animal pens (Deane, 1956). It has iments on host choice by Lu.longipalpis females resolving the questions of (1) whether or not they have host pre• Corrcspondcnce: DrC. Dyc, Vector Biology and Epidemiology ferences, either innate or facultative; if so (2) whether host Unit. Department of Medicai Parasitology. London School of preferences vary from one population to another. Such Hygiene and Tropical Medicine, Keppel Street. London WCIE variation might be expected, as Lu.longipalpis, sensu lato, 7HT, U.K. is known to exist as a complex of at least two species. 195 196 R. J. Quinnell, C. Dye and J. J. Shaw which are reproductively isolated froni each other and different host individuais, except that only one dog was which produce different pheromone compounds (Ward used in ali four replicates at Albino. Hosts were rotated et al., 1983, 1988). Both species occur in NE and S Brazii, between chicken sheds each night (position 1 i'. 2), such whiie only one occurs in the Amazon region, and it has that a different host species was present in any one chicken been suggested that interspecific differences in the degree shed each night. of anthropophily may help explain the distribution of At the end of each replicate the number, sex and species human AVL disease in Brazil (Ward et al., 1983, 1985). of ali sandflies trapped was recorded. Male and female In this paper we focus on question (1) above, reporting Lu.loiigipalpis were routinely identified from externai the results of a series of experiments designed to deter• morphology; doubtful females were dissected and sper- mine the innate host preferences of Lu.longpalpis on mathecae examined. Marajó Island in Amazonian Brazil. Three host species Experiment 2. This experiment compared the attract• were used: humans, dogs and chickens, the iatter being iveness of a boy and a group of chickens; only two chicken the most abundant domestic animal in the region. The sheds at each site were used. The boy was in one shed and work is the first step towards explaining why, on Marajó chickens were in the other, either twelve (Campinas) or six Island, seroprevalence of AVL in the human population to seven (Albino). Experimental details were otherwise is very much lower (<2%) than it is in the dog population unchanged. Experiments were repeated six times at (around 50%: unpublished data, Wellcome Parasitology Campinas (using three different boys) and four times at Unit, Belém). Albino (two different boys), the position of the hosts being swapped in each replicate. Human-biting catches. These were carried out at the Materials and Methods Campinas house. R.J.Q. and J.J.S. sat 4m from the main chicken shed for 1 h between 18.40 and 20.40 hours on Study area. Field experiments were carried out in two three consecutive nights in May 1991. Ali biting female viilages (Campinas and Albino) in Salvaterra district, fiies were collected at the time of biting; at the end of the Marajó Island, Pará State, Brazil (0°46'S, 48°31'W). hour as many settled male flies as possible were also col• This is an area of savannah and open woodiand, with oc- lected. On the first night only, ali chickens were removed casional patches of seasonally flooded forest. The human from the chicken shed beforehand. population consists mostiy of farmers; pineappics are an Laboratory experiment (Experiment 3). This experiment important cash crop. Houses are usually constructcd of used first generation laboratory bred Lu.longipalpix from mud on a wooden frame, with a palm-thatched roof. Most a colony at the Wellcome Parasitology Unit, Belém, which houses also have a chicken shed nearby, made of wooden had been established with wild-caught female flies from stakes driven into the ground, with a paim roof. Houses Marajó. Flies used were ali females, 1-7 days old, and generally have one or more dogs; cats and pigs are also had been offered sucrose solution only. present in smaller numbers. Laboratory experiments were Single humans, dogs or chickens were placed in pairs carried out in Salvaterra town. Ali experiments were 1.5 m apart inside a large, sandfly-proof net sized 2 x 1.4 x carried out between April and December 1991. 1.4m. Dogs and chickens were constrained in metal cages. Field experiments. These were carried out in the back- Ali humans were adult males aged 25-45 years. Fifteen yards of two houses, one each in Campinas and Albino. to fifty-three female flies were then released into the net At each site, four new chicken sheds were constructed, and recaptured after Ih. Five replicates of each host each 1 X 1 X 1.5 m. The sides and raised floor of the sheds combination were carried out, on different days and using were made of 2 x 1 cm timber; the roof was thatched with different host individuais. Ali experiments were carried palm leaves. The sheds were placed in a semi-circular out between 20.00 and 23.30 hours. arrangement, 4m from the existing chicken shed, and 4m Engorged flies were squashed onto a glass microscopc (Campinas) or 6m (Albino) from each other. slide (chicken versus man/dog comparisons) or blotted Experiment I. This experiment was designed to test the onto filter paper (man versus dog comparisons). Slides relative attractiveness of three host species: human, dog were stained with Giemsa and examined under 400x and chicken. Hosts were borrowed from nearby houses magnification for the presence of nucleated erythrocytes. with the consent of their parents or owners, and were Filter papcrs were stored at room temperature in plastic protected with sandfiy-proof netting during the experiment. bags containing desiccant and transported to the U.K. Ali human participants were 9-15-year-old boys. Scra were then eluted and the bloodmeal identified by At the start of the experiment (between 18.(K) and ELISA using standard techniques (Service et al., 1986). 19.30 hours) an individual of each host species was placed in each chicken shed; the fourth shed was left empty. A CDC miniature light-suction trap was placed in the Results apex of each shed, and the resident chickens removed Experiment l from the original chicken shed (except for one brooding hen).