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Natural breeding places of phlebotomine sandflies
M. D. FELICIANGELI
´ Universidad de Carabobo, Facultad de Ciencias de la Salud, Centro Nacional de Referencia de Flebotomos, BIOMED, Nucleo Aragua, Maracay, Venezuela ´
Abstract. Methods of finding larvae and pupae of phlebotomine sandflies (Diptera: Psychodidae) are described and the known types of breeding sites used by sandflies are listed. Three ways of detecting sandfly breeding places are the use of emergence traps placed over potential sources to catch newly emerged adult sandflies; flotation of larvae and pupae from soil, etc., and desiccation of media to drive out the larvae. Even so, remarkably little information is available on the ecology of the developmental stages of sandflies, despite their importance as vectors of Leishmania, Bartonella and phleboviruses affecting humans and other vertebrates in warmers parts of the world. Regarding the proven or suspected vectors of leishmaniases, information on breeding sites is available for only 15 out of 29 species of sandflies involved in the Old World and 12 out of 44 species of sandflies involved in the Americas, representing $3% of the known species of Phlebotominae. Ecotopes occupied by immature phlebotomines are usually organically rich moist soils, such as the rain forest floor (Lutzomyia intermedia, Lu. umbratilis, Lu. whitmani in the Amazon; Lu. gomezi, Lu. panamensis, Lu. trapidoi in Panama), or contaminated soil of animal shelters (Lu. longipalpis s.l. in South America, Phlebotomus argentipes in India; P. chinensis in China; P. ariasi, P. perfiliewi, P. perniciosus in Europe). Developmental stages of some species (P. langeroni and P. martini in Africa; P. papatasi in Eurasia; Lu. longipalpis s.l. in South America), have been found in a wide range of ecotopes, and many species of sandflies employ rodent burrows as breeding sites, although the importance of this niche is unclear. Larvae of some phlebotomines have been found in what appear to be specialized niches such as Lu. ovallesi on buttress roots of trees in Panama; P. celiae in termite hills in Kenya; P. longipes and P. pedifer in caves and among rocks in East Africa. Old World species found as immatures in the earthen floor of human habitations include P. argentipes, P. chinensis, P. martini and P. papatasi. Much more information on sandfly breeding sites is required to facilitate their control by source reduction. Key words. Leishmania, Lutzomyia, Phlebotomus, Sergentomyia, emergence traps, flotation methods, leishmaniasis vectors, sandfly breeding sites, sandfly ecology, source reduction, vector control.
Introduction Since the review by Killick-Kendrick (1990), important advances have been made in understanding the biology of phlebotomine sandflies and their vector roles for bartonelCorrespondence: Dr M. Dora Feliciangeli, Centro Nacional de ´ Referencia de Flebotomos (CNRFV), BIOMED, Facultad de Ciencias de la Salud, Universidad de Carabobo, Apdo. 4873, Nucleo Aragua, Maracay, Venezuela. E-mail: email@example.com ´
losis (Birtles, 2001), flaviviruses, orbiviruses, phleboviruses and vesiculoviruses (Comer & Tesh, 1991; Ashford, 2001) as well as leishmaniases (WHO, 1990; Killick-Kendrick, 1999), but knowledge of sandfly breeding sites remains scanty. Searching for developmental stages of sandflies in their natural biotopes is difficult, tedious and has proved to be remarkably unproductive (Deane & Deane, 1957; KillickKendrick, 1987, 1999). The deficit of information on sources of sandflies prevents us avoiding such sites and disallows the targeting of control measures against the
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72 M. D. Feliciangeli preimaginal stages of sandflies. Hence the only feasible countermeasures (Alexander & Maroli, 2003) depend on adult sandfly control and personal protection. The finding of a sandfly larva by Grassi (1907), in a cellar in Rome, led to the description of a new species: Phlebotomus mascittii Grassi 1908. This is regarded as the first report of an immature stage of any phlebotomine sandfly in nature. In the New World, the first findings of phlebotomine breeding sites were at the base of a tree in Brazil, where Ferreira et al. (1938) found four larvae, and Pifano (1941) found a dozen larvae in a wall of a house in Venezuela. This review gathers the scattered reports of methods used effectively to detect sandfly breeding sites, or lack of them, and summarizes the limited information available on the places from which phlebotomine larvae and pupae have been recovered. In particular, the known breeding sites of proven or suspected vectors of Leishmanias in the Old World (Table 1) and the New World (Table 2) are described, together with experiences of control efforts aimed at sandfly immature stages. Hanson (1961, 1968) modified McCombie-Young’s method by using a combination of flotation with a saturated sugar solution and washing the material through brass gauze sieves (screening-flotation technique): this led to collection of 2258 larvae of phlebotomines from the forest floor in Panama during 4 years of intensive work. Unfortunately, only 27% could be reared to the adult stage and identified, mostly as Lutzomyia longipalpis (Table 2). Soil extraction using the technique of MacFadyen (1961), based on larval escape from desiccation with warming, was employed by Seyedi Rashti & Nadim (1972) to recover Phlebotomus papatasi larvae in Iran. Also with this method, Killick-Kendrick (1987) processed 130 kg of negative sam´ ples from a goat cellar in Cevennes, France. Afterwards he tested this technique in the laboratory, demonstrating its efficiency for recovering good proportions of young larvae from soil samples seeded with laboratory-reared phlebotomine larvae. The soil incubation technique for rearing-out phlebotomine immatures to the adult stage for species identification has been widely employed in China (Y.J. Leng, personal communication). Mutinga & Kamau (1986) considered this method to be better than any other for their searches in Kenya. A wide range of trap designs have been employed to capture adult sandflies emerging from sites regarded as suitable for development of immatures, i.e. the ‘armadilha’ (1.8 m high Â 1.2 m wide) used by Deane & Deane (1957) and ground photo-collectors covering 1 m2 (Penny & Arias, 1982) in the Brazilian Amazon; traps of 0.5 m2 area for sampling of the forest floor by Rutledge & Ellenwood ´ (1975a) in Panama; small plastic bowls (0.1 m2) of Bettini et al. (1986), recently modified by Casanova (2001), and the simple polyvinyl chloride (PVC) pipe and couplings of different sizes employed by Ferro et al. (1997) in Colombia, cut so that the couplings would face available light. Emergence traps allow estimates of population density from the observed productivity of breeding sites, expressed as adults/area/time (Southwood, 1966). ´ Despite controversies over soil ecology (Andre et al., 2002), the use of radiography (Villani & Gould, 1986; Villani et al., 1989) to investigate the behaviour of scarab grubs in soil may point to ways of observing radio-labelled phlebotomine immatures under semi-natural conditions in their breeding sites.
Methods of searching for immature stages of phlebotomines Besides the occasional finding of sandfly larvae and pupae in nature, four main methods have been employed to search systematically for sandfly developmental stages in potential ecotopes. 1 Direct visual searches of materials (e.g. fungi, leaf litter, soils) sampled from potential habitats and examined under a stereomicroscope. 2 Soil extraction, using flotation with saturated solutions of sugar or salt, or desiccation to drive out the larvae. 3 Soil incubation, i.e. waiting for adult sandflies to emerge. 4 Use of emergence traps (cages) and sticky traps (oil papers) over potential breeding sites of sandflies. During the early decades of the 20th Century, in the quest for sandfly breeding places, substantial efforts were made to find phlebotomine larvae and pupae by directly searching various types of natural habitats in several countries, i.e. Malta (Marrett, 1910, 1913, 1915; Newstead, 1912; Wittingham & Rook, 1923), India (Howlett, 1913; Mitter, 1919) and Sudan (King, 1913, 1914) as well as Italy. Although more difficult and time-consuming than the other methods, Dhiman et al. (1983) still preferred direct searches for recovering immature stages of Phlebotomus argentipes from soil litter in human dwellings and cattle sheds in Bihar, India. The flotation method introduced in India by McCombieYoung et al. (1926) was claimed to hasten the extraction of sandfly larvae from soil, but required no less effort, nor were striking results achieved. As an example of the low but precious yield of phlebotomine immatures obtained by flotation, Petrishcheva & Izyumskaya (1941) recovered 61 larvae and 91 pupae from 6 tons of soil processed in Sebastopol, Crimea, U.S.S.R.
Breeding sites of phlebotomine sandflies Hanson (1968) stated that the location of breeding sites of phlebotomine sandflies was often merely assumed, because of the proximity of adult resting places. By investigation, he detected immature stages of phlebotomines in only 53% of the suspected breeding places he explored. Killick-Kendrick (1987) suggested that, as for other Diptera, sandflies would not lay eggs indiscriminately: they must recognize suitable sites for larval development. Subsequent papers on sandlfy oviposition attractants/stimulants (El Naiem & Ward, 1992)
2004 The Royal Entomological Society, Medical and Veterinary Entomology, 18, 71–80
Table 1. Studies on breeding sites of proven or suspected vectors of leishmaniases in the Old World: species and habitats according to Killick-Kendrick (1999). Clinical forms: ACL, anthroponotic cutaneous; CL, cutaneous; DCL, diffuse cutaneous; PKDL, post kala-azar dermal; VL, visceral; ZCL, zoonotic cutaneous. Methods. DS, direct searching; ET, emergence traps (number of sticky papers: nights); FS, flotation with sugar solution; SD, soil desiccation; SI, soil incubation; Sites: AB, animal burrow (#Apodemus; yrodent); AS, domestic animal shelter; CG, cellar with goats; CS, cattle shelter; GO, ground outdoors; HH, human habitations; HS, horse stables; RD, refuse dump; FR, floor of room; PS, poultry shed; SL, soil and litter; SP, stone pile; SS, sheep shelter; TM, termite hill; TR, tree-hole; various (ztree-holes and roots, stone cracks, latrine, walls; **cave, latrine, under bridge). Habitats: D, domestic; E, peridomestic; S, silvatic. References: ECB/CAMS, East China Branch of the Chinese Academy of Medical Sciences; ECKI, East China Kala-azar Institute. No, number obtained: A, adults; P, pupae; L, larvae; þ present. Vectors *proven Country: area India: Assam FS – HH, HS D, E þ – Sites Noþ/samples (%): Method material weight No. Habitat flies No. spp. References
VL, PKDL P. argentipes*
India India India E E E E
VL P. martini*
VL P. celiae* P. ariasi* ´ France: Cevennes
2004 The Royal Entomological Society, Medical and Veterinary Entomology, 18, 71–80 FS DS FS SI ET SI SI SI SI SI SI ET(120) P. perfiliewi* P. langeroni* Italy: Tuscany Italy: Sardinia Italy: Sardinia Egypt: El Agamy, Alexandria SD DS DS SD ET ET ET ET(11) E D, D, D, D, S S D S S S E E E S S S E S S E P. tobbi P. chinensis Jiangsu Shandong Jianchang, Liaoning, Suizhong Greece China: Jiangsu DS DS DS 4/75 (5%) 10/102 (10%) 15/131 (12%) 38/157 (24%) – 109/150 (73%): 1859 kg 80/114 (70%): 1602 kg 25/54 (42%): 230 kg 25/44 (57%): 172 kg 109/150 (73%): 1858 kg 25/44 (57%): 172 kg – – 1/6 (17%) – 77 kg 130 kg – 18/25 (72%) 18/25 (72%) – – – – – – 20% D 10% 54/2808 (2%) 1/4 (25%) AS Variousz ABy E E D þ þ þ – – – – CS CS, HH HH CS CS TM AB HH TR TM TR RD CG CG AB# SL SL AS SS AS Various SP AS ABy RD Wells FR 1P 2A, 6P, 50L 11L, 8P 38A 69A 41A 19A 5A 2A 1A 1A 5A 1A 6L 0 0L 0L 19A 83A 3731A 115A 39A 23A 1A 3A þ þ – 3 – – – 17 14 9 10 – – 1 – – – – – 2 2 3 – – – – – – – Shortt et al., 1930, 1932; Smith et al., 1936 (in Hanson, 1961) Pandya & Niyogi, 1980 Dhiman et al., 1983 Ghosh & Bhattacharya 1991 Ghosh & Bhattacharya 1991 Ghosh & Bhattacharya 1991 Mutinga et al., 1989 Mutinga et al., 1989 Mutinga et al., 1989 Mutinga et al., 1989 Mutinga et al., 1989 Mutinga et al., 1989 Killick-Kendrick, 1987 Killick-Kendrick, 1987 Killick-Kendrick, 1987 Killick-Kendrick, 1987 Killick-Kendrick, 1987 Killick-Kendrick, 1987 Pozio et al., 1983 Bettini, 1989 Bettini, 1989 Doha et al., 1990 Doha et al., 1990 Doha et al., 1990 Doha et al., 1990 Doha et al., 1990 Biocca & Costantini, 1986 CAMS 1952 (unpubl.) ECB/CAMS & ECKI 1954 (unpubl.) ECB/CAMS & ECKI 1954 (unpubl.) Leng, 1956 (pers. com.) Nicolescu & Bilbie, 1980
Breeding places of phlebotomine sandflies 73
74 M. D. Feliciangeli
Table 1. Continued. Vectors *proven Country: area Sites Noþ/samples (%): Method material weight No. Habitat flies No. spp. References
ACL ZCL ZCL
– – 1.3 kg 80/114 (70%): 1602 kg 191/423 (45%) 4/75 (5%) 10/102 (10%)
Rocks Caves ABy ABy FR, GO CS, HH CS, HH CS, HH ABy ABy, CS
1A 0 4A 2A þ 5L 5L 4L þ
P. sergenti* Romania P. guggisbergi* Kenya P. duboscqi* Senegal Kenya DCL, ZCL P. papatasi* India Assam India India: Bilhar Central Asia Central Asia Iran Egypt: Alexandria 7/226 (3%)
ET SI SI SI FS FS FS DS ET ET, FS SD ET(11)
Egypt Ethiopia Kenya 43.5 kg
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Le. aethiopica ZCL, DCL P. longipes* P. pedifer*
S S S E D, E E E D, E E D, S E Various E SP E AS D ABy E RP E ABy E PS E Various** E Caves E A115 A28 A18 A2 A1 þ þ 15L 13P
1 – 1 17 – – – 3 – – – 2 – – – – – – 2 –
Nicolescu & Bıˆ lbıˆ e, 1980 Mutinga, 1996 Dedet et al., 1982 Mutinga et al., 1989 McCombie-Young et al., 1926 Smith et al., 1936 Pandya & Niyogi, 1980 Dhiman et al., 1983 Perfil’ev, 1968 Artemiev et al., 1972 Seyedi Rashti & Nadim, 1972 Doha et al., 1990 Doha et al., 1990 Doha et al., 1990 Doha et al., 1990 Doha et al., 1990 Morsy et al., 1993 Morsy et al., 1993 Foster, 1972 Mutinga & Odhiambo, 1986
Table 2. Studies on breeding sites of Lutzomyia spp., proven or suspected vectors of leishmaniases in the New World (species according to Killick-Kendrick, 1999). A, adult sandflies; CL, cutaneous leishmaniasis; ET, emergence traps (number of trap-nights); L, sandfly larvae; MCL, muco-cutaneous leishmaniasis; VL, visceral leishmaniasis. Vectors *proven Country: area Salt-flotation 7A 11A 3A 1A 3 3 3 3 12/241 (5%) 12A 1 Method ´ Lu. longipalpis s.l.* Brazil: Ceara Noþ/samples (%): Sites: proportion þ material weight or rate of production No. flies No. spp. References Deane & Deane, 1957 Deane & Deane, 1957 Ferro et al., 1997 Ferro et al., 1997 Ferro et al., 1997 Hanson, 1961, 1968
Le .i. chagasi
Colombia: Cundinamarca ET(232) ET(25) ET(288) Panama Canal Zone Screen-flotation 88/370 (24%)
animal corrals 2/15 (13%) among rocks 6/50 (12%) Pig-pens (5 flies/100 m2) tree trunks (1.63 flies/100 m2) rocks (1.42 flies/100 m2) forest floor dead leaves
Le. panamensis CL, MCL Lu. Lu. Lu. Lu. Lu. Lu. gomezi panamensis ylephiletor trapidoi* trapidoi* ovallesi* Direct exam
forest floor buttressed roots
600A, 2258L 15 8A 2A 12A 39A 24A
2004 The Royal Entomological Society, Medical and Veterinary Entomology, 18, 71–80 Lu. trapidoi* panamensis gomezi ylephiletor umbratilis* Brazil: Central Amazon Brazil: Central Amazon Brazil: Central Amazon Brazil: Sao Paulo ET(243) ET(243) Soil incubation ET(243) ET (2061) leaf litter (24.4 flies/100 m2/day) 307A 90A 33A 28A 40A forest floor (4.1-14 s/100m2/day) 6 15 s.l. s.l. s.l. s.l. Brazil: Espirito Santo Brazil: Sao Paolo 1/1 1/1 1/1 Soil incubation ET ET ET ET ET anduzei* paraensis intermedia intermedia pessoai intermedia whitmani* intermedia 55A 2A 12A 1A 1A 6A 7A 39A 1 1 1 3 3 Forattini, 1954 Vieira et al., 2000 Casanova, 2001 Lu. intermedia s.l. Lu. pessoai pig-shed forest floor forest floor Soil forest floor forest floor (32.6-38.7 s/100m2/day) forest floor 25A (24 s/100m2/day) 2A
Hanson, 1961, 1968; Rutledge & Mosser, 1972 Rutledge & Ellenwood, 1975b, c
Lu. Lu. Lu. CL, MCL Lu.
Arias & Freitas, 1982
Breeding places of phlebotomine sandflies
CL, MCL Lu. Lu. Le. braziliensis CL, MCL Lu. Lu. Lu. Lu. Lu. Lu.
76 M. D. Feliciangeli produced by the accessory glands (Dougherty et al., 1992) and the response of gravid females to compounds emitted by faeces of chicken or rabbit (Dougherty et al., 1995), as well as to soil bacteria isolated from natural breeding sites in India (Radjame et al., 1997), support such a hypothesis. Tables 1–3 list the sites in domestic, peridomestic and silvatic habitats from which sandfly pre-imaginal stages have sometimes been recovered. However, based on the frequency of the collections and the abundance of specimens caught, only a few of them might be considered as stable breeding sites. Human dwellings and cattle sheds in India and gerbil burrows in Central Asia (Perfil’ev, 1968) may be regarded as stable breeding sites of Phlebotomus papatasi. Developmental stages of P. duboscqi were recovered from burrows of the giant African cane rat, Cricetomys gambianus, by Dedet et al. (1982) and from unidentified rodent burrows in Kenya (Mutinga et al., 1986), Phlebotomus martini was found to breed mainly in animal burrows, whereas termite hills were regarded as secondary breeding sites in Kenya (Mutinga et al., 1989).
Table 3. Summary of situations from which immature stages of phlebotomine sandflies have been recovered Habitat Domestic Ectotope Abandoned buildings Basements and cellars of houses Cracks in mud floors and walls Soil in human dwellings Animal burrows Animal shelters (cattle, pigs) Caves Chicken coops Debris and soil cracks Dry excreta of small domestic animals Earth dyke Embankments Latrines Rotted manure Rubbish in the street Soil at the base of old walls Under stones Wells Ant nests Burrows of gerbil and other rodents Burrows of other animals (unknown) Caves Cesspits, dry Drains Garbage Hollow trees Leaf litter on forest floor Nests of terrestrial tortoises Nests of birds Rocks, between and under Roots of large trees Soil at base of trees Soil under overhanging rocks Termite hills
Research on the breeding sites of sandfly vectors of leishmaniases Studies on potential breeding sites of proven and suspected vectors of leishmaniases are summarized in Table 1 for the Old World and Table 2 for the New World, in relation to the Leishmania parasites they transmit, the locality, methods used and data on the work effort, if available. The source of samples studied and the habitat (domestic, peridomestic or silvatic) are given. Results are expressed as the proportions of positive samples among those processed, the amount of material screened and/or the numbers of positive and total emergence traps used. The number and stage(s) of specimens recovered (larvae or pupae) and the number of species found are also reported with the source reference. For the known and suspected sandfly vectors of the important leishmaniases (WHO, 1990), immature stages have been recovered for at least 7 out of 10 proven vectors of Leishmania donovani s.l and Le. infantum in the Old World, as follows with their references: P. argentipes (Shortt et al., 1930, 1936; Smith et al., 1936; Pandya & Niyogi, 1980; Dhiman et al., 1983; Ghosh & Bhatthacharya, 1991), P. celiae and P. martini (Mutinga & Kamau, 1986; Mutinga et al., 1989), P. ariasi (Killick-Kendrick, 1987), P. perfilievi and P. perniciosus (Pozio et al., 1980; Bettini et al., 1986; Bettini & Melis, 1988) and P. langeroni (Doha et al., 1990). Immature stages of P. tobbi, suspected vector of Le. infantum around the eastern Mediterranean and Sicily, were detected in wells on the island of Zakinthos, Greece (Biocca & Costantini, 1986). According to Professor Yan Jia Leng (personal communication), larvae and pupae of P. chinensis have been detected in several ecotopes (Table 1) during extensive work on leishmaniasis and its vectors by the East China Branch of the Chinese Academy of Medical Sciences (ECB/CAMS) and the East China Kala-azar Institute (ECKI).
Only two species of sandfly, P. argentipes in India and P. chinensis in China, have been encountered repeatedly in soil samples in the earth floor of human dwellings and cowsheds, whereas only small proportions of the larvae and pupae of P. martini in Kenya have been found in the houses. Mutinga & Kamau (1986) and Mutinga et al. (1989) stated that the main breeding sites of this species are animal burrows and termite hills, which serve as incubators with well regulated internal environments. Of the closely related P. celiae in Kenya, they found only two males (from a tree-hole and a termite hill), insufficient to reveal much about the breeding sites of this species. In southern Ethiopia, however, Leishmania-infected P. martini and P. celiae have been recovered from termite hills, suggesting that termite galleries may provide an important ecotope for the epidemiology of Le. donovani, the aetiological agent of kala-azar (Gebre-Michael & Lane, 1996). Poor results were obtained from searching for the breed´ ing sites of P. ariasi in the Cevennes focus of Leishmania infantum, causing canine and human visceral leishmaniasis in France. However, Killick-Kendrick (1987) reached the conclusion that the larval ecotopes of P. ariasi are probably domestic and have a high content of organic matter.
2004 The Royal Entomological Society, Medical and Veterinary Entomology, 18, 71–80
Breeding places of phlebotomine sandflies The findings of Bettini (1989) in Sardinia were, as he wrote, ‘surely exceptional’. An abandoned cement structure (area 25 m2), used as a sheep shelter, was found to be productive of three species of sandfly: Sergentomyia minuta and two species of Phlebotomus (Bettini et al., 1986). After sealing the shelter, they collected totals of 23 338 P. perfiliewi and 1309 P. perniciosus with six exit traps during 1983– 1985 (Bettini, 1989). Analysis of the substrate soil for texture, pH, CaCO3, organic matter and water content showed no correlation with the number of sandflies that emerged from the spots where soil samples were taken. Apparently the developmental stages were associated with a relatively stable, cool and humid environment protected from sunshine and rain, rich in clay and organic nitrogen. Sampling from a similar site in Tuscany, however, yielded very few specimens of these species (Pozio et al., 1980). Immature stages of P. langeroni were found in Egypt (Doha et al., 1990), mainly in rubbish from stone piles. About the vectors of Le. tropica causing cutaneous leishmaniasis, Mutinga & Odhiambo (1986) claimed that P. guggisbergi breeds in Kenyan caves. In Romania, surveys of potential sandfly biotopes at Dobrudja, using oil papers, yielded only one P. sergenti (Nicolescu & Bıˆ lbıˆ e, 1980), although that species was formerly abundant in Canaraua Fetii rocks (Duport et al., 1971). The decrease of P. sergenti may be attributed to geological exploitation, spoiling the sandfly breeding sites (Nicolescu & Bıˆ lbıˆ e, 1980). Regarding the most widespread form of cutaneous leishmaniasis, caused by Leishmania major, the predominant vector Phlebotomus papatasi is well known and apparently not complex (Parvizi et al., 2003): information on breeding sites of this sandfly is available from several countries (Table 1). In India, immature stages of P. papatasi have been recovered consistently from cattle sheds and human dwellings in urban areas (McCombie-Young et al., 1926; Smith et al., 1936; Pandya & Niyogi, 1980; Dhiman et al., 1983). In rural areas they have been found in various habitats: unused poultry houses made of bricks and clay, manure heaps, caves, embankments, dried-up cesspits and latrines (Sivagnaname & Amaldraj, 1997). In Egypt, breeding sites of P. papatasi have been found in a similar range of ecotopes (Artemiev et al., 1972; Doha et al., 1990). In the Central Asian Republics of the former Soviet Union, burrows of the desert gerbil (Rhombomys opimus) are recognized as breeding sites of this sandfly species (Perfil’ev, 1968; Artemiev et al., 1972). Towards the equator, Dedet et al. (1982) in Senegal and Mutinga et al. (1986) in Kenya found P. duboscqi, the Afrotropical vector of L. major, breeding in animal burrows. Caves were implicated as probable breeding sites of P. longipes and P. pedifer, proven vectors of Le. aethiopica, studied by Foster (1972) in Ethiopia and by Mutinga & Odhiambo (1986) in Kenya. Far less is known about the breeding sites of phlebotomine sandfly vectors in the New World. Research on this subject during a period of 20 years (1940–1960) yielded only $60 specimens of immature phlebotomines (Hanson, 1961). Among these, 19 were Lutzomyia longipalpis s.l., the main
vector of American visceral leishmaniasis, recovered by Deane & Deane (1957) from animal corrals and among rocks in Brazil. Those workers stressed the discrepancy between the abundance of Lu. longipalpis adult sandflies, which they said were ‘found everywhere’ in the State of ´ Ceara, Brazil, and the rarity of finding the pre-imaginal stages. Similar results were obtained 40 years later in Colombia, where more immatures were recovered from animal sheds close to houses rather than from isolated microhabitats (Ferro et al., 1997). No information is available on the breeding sites of Lu. evansi, a proven vector of Leishmania infantum chagasi in Colombia (Travi et al., 1990) and Venezuela (Feliciangeli et al., 1999). In undisturbed Neotropical forests, where vector sandflies are closely associated with the wild animal reservoirs of Leishmania spp., pre-imaginal stages have been obtained for 10 out of 42 proven or suspected vectors of cutaneous leishmaniasis (Killick-Kendrick, 1999). Notably, Lutzomyia gomezi, Lu. ovallesi, Lu. panamensis, Lu. trapidoi and Lu. ylephiletor were all caught emerging from the forest floor in ´ Panama (Hanson, 1968). Moreover, Rutledge & Ellenwood (1975a,b) pointed out that plant–sandfly interactions largely determine the pattern of sandfly production in or on the forest floor habitat; thus, Lu. trapidoi was associated with large lianas (Ouruparia and Sabicea), whereas Lu. panamensis and Lu. gomezi were associated with large Anacardium trees. No plant association was established for Lu. ovallesi, although its larvae were found between tree buttresses (Hanson, 1968; Rutledge & Mosser, 1972). It was inferred that Lu. ovallesi seeks out these sheltered places for oviposition, as adults seldom use these habitats for daytime resting places (Rutledge & Ellenwood, 1975a,b). This behaviour of Lu. ovallesi was also observed in north-central Venezuela (Feliciangeli, 1987) where this species is the main vector of cutaneous leishmaniasis (Feliciangeli & Rabinovich, 1998). Arias & Freitas (1982) caught Lu. anduzei and Lu. umbratilis, emerging from the ‘terra firme’ forest floor in the central Amazon region of Brazil (Table 2). However, they concluded that the open forest floor is not one of the major breeding sites for these sandflies. Breeding sites of Lu. whitmani and Lu. intermedia have been detected more often in the peridomestic than the silvatic habitat (Table 2), as demonstrated by Casanova (2001) in rural areas of the Mogy Guacu River, Brazil. ¸ This tendency may be linked with changing epidemiological patterns in the transmission of American cutaneous leishmaniasis (ACL), increasing risk factors being associated with peri- and intradomiciliary habitats (Campbell-Lendrum et al., 2001; Desjeux, 2001).
Controlling the immature stages of phlebotomine sandflies This topic was reviewed by Alexander & Maroli (2003). For eco-epidemiological reasons, it is important to focus on strengthening research in the detection of breeding places.
2004 The Royal Entomological Society, Medical and Veterinary Entomology, 18, 71–80
78 M. D. Feliciangeli The first attempted control aimed at immature stages of phlebotomine sandflies, using necrocene with crude oil and kerosene mixture, was applied in India by Smith et al. (1936), without much success. In the Central Asian Republics, destruction of burrows of the great gerbil (Psammomys) effectively controlled P. papatasi (Faizulin et al., 1976), whereas chemical control with organochlorine insecticides did not give such a good result (Vioukov, 1987). Larval habitat modification by plastering walls of human dwellings and cattle sheds was quite effective to control P. argentipes, the Indian vector of visceral leishmaniasis (Kumar et al., 1995). However, there were problems with the high cost of the product and its high viscosity, which made it difficult to spray. More encouragingly, selective application of the biopesticide Bacillus sphaericus (Bs) into the burrows of host rodents was successful against P. papatasi (Pener et al., 1996). The Bs toxin works as a stomach poison against target insects, but it remains unclear whether the impact was mostly on immature or adult sandflies. Spraying plants with a sugar solution of B. sphaericus, for adult sandflies to ingest and carry back to poison the larvae, reduced sandfly populations emerging from animal burrows but not those emerging from termitaria in Kenya (Robert et al., 1997). As no stable silvatic breeding sites of ACL vectors have yet been identified in the Americas, it remains impossible to target the immature stages or to attempt sandfly source reduction. Even so, some efforts to reduce sandfly populations were applied to tree-holes where they might affect immature as well as adult sandflies (Floch, 1957; Chaniotis et al., 1982; Ready et al., 1985). Perhaps entomopathogenic fungi could be used against sandfly immatures in defined areas; for example Beauveria bassiana is applied to control the coffee berry borer Hypothenemus hampei in Colombian coffee plantations. Unfortunately, a trial evaluation of B. bassiana was unsuccessful for sandfly control (Reithinger et al., 1997). Because of the increasingly close human–vector associations, giving rise to greater risks of Leishmania transmission (Dye, 1996), there is growing hope and scope for identifying restricted peridomestic breeding sites of sandflies that might be amenable to control, by larviciding or environmental modification to eliminate the source. Medicine, U.K., for kindly providing photocopies of papers not available in Venezuela.
Alexander, B. & Maroli, M. (2003) Control of phlebotomine sandflies. Medical and Veterinary Entomology, 17, 1–18. ´ Andre, H.M., Ducarme, X. & Lebrun, P. (2002) Soil biodiversity: myth, reality or conning? Oikos, 96, 3–10. Arias, J.R. & Freitas, R.A. (1982) On the vectors of cutaneous leishmaniasis in the central Amazon of Brasil. 4. Sand fly emergence from a ‘terra firme’ forest floor. Acta Amazonica, 12, 609–611. Artemiev, M.M., Flerova, O.A. & Belyaev, A.E. (1972) Quantitative evaluation of the productivity of breeding places of sandflies in the wild and in villages. Meditsinskaya Parazitologiya i Parazitarnye Bolezni, 41, 31–35. Ashford, R.W. (2001) Phlebotomus fevers. The Encyclopedia of Arthropod-Transmitted Infections (ed. by M. W. Service), pp. 397–401. CABI Publishing, Wallingford, U.K. Bettini, S. (1989) Sandfly breeding-sites. Life Sciences, 163, 179–188. Bettini, S., Contini, C., Atzeni, M.C. & Tocco, G. (1986) Leishmaniasis in Sardinia. I. Observations on a larval breeding site of Phlebotomus perniciosus, Phlebotomus perfiliewi perfiliewi and Sergentomyia minuta (Diptera: Psychodidae) in the canine leishmaniasis focus of Soleminis (Cagliari). Annals of Tropical Medicine and Parasitology, 80, 307–315. Bettini, S. & Melis, P. (1988) Leishmaniasis in Sardinia. III. Soil analysis of a breeding site of three species of sandflies. Medical and Veterinary Entomology, 2, 67–71. Biocca, E. & Costantini, R. (1986) I pozzi come possibili focolai larvali di flebotomi nell’Isola de Zante. Annali dell’Istituto ´, Superiore di Sanita 22, 59–60. ´ Birtles, R.J. (2001) Carrion’s disease. The Encyclopedia of Arthropod-Transmitted Infections (ed. by M. W. Service), pp. 104–106. CABI Publishing, Wallingford, U.K. Campbell-Lendrum, B., Dujardin, J.P., Martinez, E., Feliciangeli, M.D., Perez, J.E., Passerat de Silans, L.N.M. & Desjeux, P. (2001) Domestic and peridomestic transmission of American cutaneous leishmaniasis: changing epidemiological patterns present new control opportunities. Memorias do Instituto Oswaldo Cruz, 96, 159–162. Casanova, C. (2001) A soil emergence trap for collections of Phlebotomine sandflies. Memorias do Instituto Oswaldo Cruz, 96, 273–275. Chaniotis, B.N., Parsons, R.E., Harla, H.J. & Correa, M. (1982) A pilot study to control phlebotomine sand flies (Diptera: Psychodidae) in a neotropical rain forest. Journal of Medical Entomology, 19, 1–5. Comer, J.A. & Tesh, R.B. (1991) Phlebotomine sand flies as vectors of vesiculovirus: a review. Parassitologia, 33 (Suppl.), 143–150. Deane, L. & Deane, M.P. (1957) Observacoes sobre abrigos e ¸ ˜ ˆ ´ ´ criadouros de flebotomos no Noroeste do Estado do Ceara. Revista Brasileira de Malariologia e Doencas Tropicais, 9, ¸ 225–246. ´ Dedet, J.P., Desjeux, P. & Derouin, F. (1982) Ecologie d’un foyer ´ ´ ` ´ ´ de leishmaniose cutanee dans la region de Thies (Senegal, ´ Afrique de l’Ouest. 4. Infestation spontanee et biologie de Phlebotomus duboscqi Neveu-Lemaire 1906. Bulletin de la Socie´te´ de Pathologie Exotique, 75, 588–589.
Acknowledgements This review is dedicated to Dr Lawrence Quate, who, in 1964, processed 2500 kg of soil in Sudan to recover only a single larva of Sergentomyia africana (Quate, 1964). With the recent death of Dr Quate, we have lost one of the very few expert taxonomists of the family Psychodidae. I wish to thank Dr Philippe Desjeux for the encouragement to publish this review and his helpful criticisms, Professor Yan Jia Leng for kindly providing me information on the breeding sites of vectors of leishmaniases in China, Dr Michele Maroli of the Istituto Superiore di ´ Sanita, Roma, Italia, and Sinead Fitzpatrick, postgraduate student at the London School of Hygiene and Tropical
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Accepted 10 February 2004
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