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Medical and Veterinary Entomology (2004) 18, 71–80


Natural breeding places of phlebotomine sandflies

Universidad de Carabobo, Facultad de Ciencias de la Salud, Centro Nacional de Referencia de Flebótomos,
BIOMED, Núcleo 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 losis (Birtles, 2001), flaviviruses, orbiviruses, phleboviruses

and vesiculoviruses (Comer & Tesh, 1991; Ashford, 2001) as
Since the review by Killick-Kendrick (1990), important well as leishmaniases (WHO, 1990; Killick-Kendrick, 1999),
advances have been made in understanding the biology of but knowledge of sandfly breeding sites remains scanty.
phlebotomine sandflies and their vector roles for bartonel- Searching for developmental stages of sandflies in their
natural biotopes is difficult, tedious and has proved to be
Correspondence: Dr M. Dora Feliciangeli, Centro Nacional de remarkably unproductive (Deane & Deane, 1957; Killick-
Referencia de Flebótomos (CNRFV), BIOMED, Facultad de Kendrick, 1987, 1999). The deficit of information on
Ciencias de la Salud, Universidad de Carabobo, Apdo. 4873, sources of sandflies prevents us avoiding such sites and
Núcleo Aragua, Maracay, Venezuela. E-mail: mdora@telcel.net.ve disallows the targeting of control measures against the

# 2004 The Royal Entomological Society 71

72 M. D. Feliciangeli

preimaginal stages of sandflies. Hence the only feasible Hanson (1961, 1968) modified McCombie-Young’s
countermeasures (Alexander & Maroli, 2003) depend on method by using a combination of flotation with a satur-
adult sandfly control and personal protection. ated sugar solution and washing the material through brass
The finding of a sandfly larva by Grassi (1907), in a cellar gauze sieves (screening-flotation technique): this led to col-
in Rome, led to the description of a new species: Phleboto- lection of 2258 larvae of phlebotomines from the forest
mus mascittii Grassi 1908. This is regarded as the first report floor in Panama during 4 years of intensive work. Unfortu-
of an immature stage of any phlebotomine sandfly in nately, only 27% could be reared to the adult stage and
nature. In the New World, the first findings of phlebotomine identified, mostly as Lutzomyia longipalpis (Table 2).
breeding sites were at the base of a tree in Brazil, where Soil extraction using the technique of MacFadyen (1961),
Ferreira et al. (1938) found four larvae, and Pifano (1941) based on larval escape from desiccation with warming, was
found a dozen larvae in a wall of a house in Venezuela. employed by Seyedi Rashti & Nadim (1972) to recover
This review gathers the scattered reports of methods used Phlebotomus papatasi larvae in Iran. Also with this method,
effectively to detect sandfly breeding sites, or lack of them, Killick-Kendrick (1987) processed 130 kg of negative sam-
and summarizes the limited information available on the ples from a goat cellar in Cévennes, France. Afterwards he
places from which phlebotomine larvae and pupae have tested this technique in the laboratory, demonstrating its
been recovered. In particular, the known breeding sites of efficiency for recovering good proportions of young larvae
proven or suspected vectors of Leishmanias in the Old from soil samples seeded with laboratory-reared phleboto-
World (Table 1) and the New World (Table 2) are described, mine larvae.
together with experiences of control efforts aimed at sandfly The soil incubation technique for rearing-out phleboto-
immature stages. mine 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
Methods of searching for immature stages of Kenya.
phlebotomines A wide range of trap designs have been employed to
capture adult sandflies emerging from sites regarded as
Besides the occasional finding of sandfly larvae and pupae suitable for development of immatures, i.e. the ‘armadilha’
in nature, four main methods have been employed to search (1.8 m high  1.2 m wide) used by Deane & Deane (1957)
systematically for sandfly developmental stages in potential and ground photo-collectors covering 1 m2 (Penny & Arias,
ecotopes. 1982) in the Brazilian Amazon; traps of 0.5 m2 area for
1 Direct visual searches of materials (e.g. fungi, leaf litter, sampling of the forest floor by Rutledge & Ellenwood
soils) sampled from potential habitats and examined (1975a) in Panamá; small plastic bowls (0.1 m2) of Bettini
under a stereomicroscope. et al. (1986), recently modified by Casanova (2001), and the
2 Soil extraction, using flotation with saturated solutions simple polyvinyl chloride (PVC) pipe and couplings of dif-
of sugar or salt, or desiccation to drive out the larvae. ferent sizes employed by Ferro et al. (1997) in Colombia, cut
3 Soil incubation, i.e. waiting for adult sandflies to emerge. so that the couplings would face available light. Emergence
4 Use of emergence traps (cages) and sticky traps (oil traps allow estimates of population density from the
papers) over potential breeding sites of sandflies. observed productivity of breeding sites, expressed as
adults/area/time (Southwood, 1966).
During the early decades of the 20th Century, in the quest Despite controversies over soil ecology (André et al.,
for sandfly breeding places, substantial efforts were made to 2002), the use of radiography (Villani & Gould, 1986; Vil-
find phlebotomine larvae and pupae by directly searching lani et al., 1989) to investigate the behaviour of scarab grubs
various types of natural habitats in several countries, i.e. in soil may point to ways of observing radio-labelled phle-
Malta (Marrett, 1910, 1913, 1915; Newstead, 1912; Witting- botomine immatures under semi-natural conditions in their
ham & Rook, 1923), India (Howlett, 1913; Mitter, 1919) and breeding sites.
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 recove- Breeding sites of phlebotomine sandflies
ring immature stages of Phlebotomus argentipes from soil
litter in human dwellings and cattle sheds in Bihar, India. Hanson (1968) stated that the location of breeding sites of
The flotation method introduced in India by McCombie- phlebotomine sandflies was often merely assumed, because
Young et al. (1926) was claimed to hasten the extraction of of the proximity of adult resting places. By investigation, he
sandfly larvae from soil, but required no less effort, nor detected immature stages of phlebotomines in only 53% of
were striking results achieved. As an example of the low the suspected breeding places he explored. Killick-Kendrick
but precious yield of phlebotomine immatures obtained by (1987) suggested that, as for other Diptera, sandflies would
flotation, Petrishcheva & Izyumskaya (1941) recovered 61 not lay eggs indiscriminately: they must recognize suitable
larvae and 91 pupae from 6 tons of soil processed in Sebas- sites for larval development. Subsequent papers on sandlfy
topol, Crimea, U.S.S.R. 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.

Clinical Vectors Noþ/samples (%): No. No.

Parasite form(s) *proven Country: area Method material weight Sites Habitat flies spp. References
Le. donovani VL, PKDL P. argentipes* India: Assam FS – HH, HS D, E þ – Shortt et al., 1930, 1932;
Smith et al., 1936
(in Hanson, 1961)
India FS 4/75 (5%) CS E 1P – Pandya & Niyogi, 1980
India DS 10/102 (10%) CS, HH D, E 2A, 6P, 50L 3 Dhiman et al., 1983
India FS 15/131 (12%) HH D, E 11L, 8P – Ghosh & Bhattacharya 1991
SI 38/157 (24%) CS D, E 38A – Ghosh & Bhattacharya 1991
ET – CS D, E 69A – Ghosh & Bhattacharya 1991
VL P. martini* Kenya SI 109/150 (73%): 1859 kg TM S 41A 17 Mutinga et al., 1989
SI 80/114 (70%): 1602 kg AB S 19A 14 Mutinga et al., 1989
SI 25/54 (42%): 230 kg HH D 5A 9 Mutinga et al., 1989
SI 25/44 (57%): 172 kg TR S 2A 10 Mutinga et al., 1989
VL P. celiae* Kenya SI 109/150 (73%): 1858 kg TM S 1A – Mutinga et al., 1989
SI 25/44 (57%): 172 kg TR S 1A – Mutinga et al., 1989
Le. infantum CL, VL P. ariasi* France: Cévennes ET(120) – RD E 5A 1 Killick-Kendrick, 1987
– CG E 1A – Killick-Kendrick, 1987
SD 1/6 (17%) CG E 6L – Killick-Kendrick, 1987
DS – AB# S 0 – Killick-Kendrick, 1987
DS 77 kg SL S 0L – Killick-Kendrick, 1987
SD 130 kg SL S 0L – Killick-Kendrick, 1987

2004 The Royal Entomological Society, Medical and Veterinary Entomology, 18, 71–80
P. perfiliewi* Italy: Tuscany ET – AS E 19A 2 Pozio et al., 1983
Italy: Sardinia ET 18/25 (72%) SS S 83A 2 Bettini, 1989
Italy: Sardinia ET 18/25 (72%) AS S 3731A 3 Bettini, 1989
P. langeroni* Egypt: ET(11) – Various E 115A – Doha et al., 1990
El Agamy, Alexandria – SP 39A – Doha et al., 1990
– AS 23A – Doha et al., 1990
– ABy 1A – Doha et al., 1990
– RD 3A – Doha et al., 1990
P. tobbi Greece – Wells þ – Biocca & Costantini, 1986
P. chinensis China: Jiangsu DS 20% FR D þ – CAMS
1952 (unpubl.)
Jiangsu DS 10% AS E þ – ECB/CAMS & ECKI 1954
Shandong DS 54/2808 (2%) Variousz E þ – ECB/CAMS & ECKI 1954
Breeding places of phlebotomine sandflies

Jianchang, Liaoning, 1/4 (25%) ABy D þ – Leng, 1956 (pers. com.)

Suizhong – Nicolescu & Bilbie, 1980
74 M. D. Feliciangeli

Table 1. Continued.
Clinical Vectors Noþ/samples (%): No. No.
Parasite form(s) *proven Country: area Method material weight Sites Habitat flies spp. References
Le. tropica ACL P. sergenti* Romania ET – Rocks S 1A 1 Nicolescu & Bı̂lbı̂e, 1980
ZCL P. guggisbergi* Kenya SI – Caves S 0 – Mutinga, 1996
Le. major ZCL P. duboscqi* Senegal SI 1.3 kg ABy S 4A 1 Dedet et al., 1982

Kenya SI 80/114 (70%): 1602 kg ABy E 2A 17 Mutinga et al., 1989
DCL, ZCL P. papatasi* India FS FR, GO D, E þ – McCombie-Young et al., 1926
Assam FS 191/423 (45%) CS, HH E 5L – Smith et al., 1936
India FS 4/75 (5%) CS, HH E 5L – Pandya & Niyogi, 1980
India: Bilhar DS 10/102 (10%) CS, HH D, E 4L 3 Dhiman et al., 1983
Central Asia ET ABy E þ – Perfil’ev, 1968
Central Asia ET, FS ABy, CS D, S – Artemiev et al., 1972
Iran SD 7/226 (3%) E – Seyedi Rashti & Nadim, 1972
Egypt: Alexandria ET(11) Various E A115 2 Doha et al., 1990
SP E A28 – Doha et al., 1990
AS D A18 – Doha et al., 1990
ABy E A2 – Doha et al., 1990
RP E A1 – Doha et al., 1990
Egypt ET ABy E þ – Morsy et al., 1993
ET PS E þ – Morsy et al., 1993
Le. aethiopica ZCL, DCL P. longipes* Ethiopia FS 43.5 kg Various** E 15L 13P 2 Foster, 1972
P. pedifer* Kenya SI Caves E – Mutinga & Odhiambo, 1986

2004 The Royal Entomological Society, Medical and Veterinary Entomology, 18, 71–80
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.

Clinical Vectors Noþ/samples (%): Sites: proportion þ No. No.

Parasite form(s) *proven Country: area Method material weight or rate of production flies spp. References
Le .i. chagasi VL Lu. longipalpis s.l.* Brazil: Ceará Salt-flotation 12/241 (5%) animal corrals 12A 1 Deane & Deane, 1957
2/15 (13%)
among rocks 7A 3 Deane & Deane, 1957
6/50 (12%)
Colombia: Cundinamarca ET(232) Pig-pens 11A 3 Ferro et al., 1997
(5 flies/100 m2)
ET(25) tree trunks 3A 3 Ferro et al., 1997
(1.63 flies/100 m2)
ET(288) rocks 1A 3 Ferro et al., 1997
(1.42 flies/100 m2)
Le. panamensis CL, MCL Lu. gomezi Panama Canal Zone Screen-flotation 88/370 (24%) forest floor 600A, 2258L 15 Hanson, 1961, 1968
Lu. panamensis dead leaves 8A
Lu. ylephiletor 2A
Lu. trapidoi* 12A
Lu. trapidoi* Direct exam forest floor 39A
Lu. ovallesi* buttressed roots 24A Hanson, 1961,
1968; Rutledge
& Mosser, 1972
Lu. trapidoi* ET (2061) leaf litter 307A 6 Rutledge
(24.4 flies/100 m2/day) & Ellenwood, 1975b, c
Lu. panamensis 90A
Lu. gomezi 33A
Lu. ylephiletor 28A

2004 The Royal Entomological Society, Medical and Veterinary Entomology, 18, 71–80
CL, MCL Lu. umbratilis* Brazil: Central Amazon ET(243) forest floor 40A 15 Arias & Freitas, 1982
(4.1-14 s/100m2/day)
Le. guyanensis CL, MCL Lu. anduzei* Brazil: Central Amazon ET(243) 55A
Lu. paraensis Brazil: Central Amazon ET(243) 2A
Le. braziliensis CL, MCL Lu. intermedia s.l. Brazil: Sao Paulo Soil incubation 1/1 pig-shed 12A 1 Forattini, 1954
Lu. intermedia s.l. 1/1 forest floor 1A 1
Lu. pessoai Soil incubation 1/1 forest floor 1A 1
Lu. intermedia s.l. Brazil: Espirito Santo ET Soil 6A 3 Vieira et al., 2000
Lu. whitmani* Brazil: Sao Paolo ET forest floor 7A 3 Casanova, 2001
Lu. intermedia s.l. ET forest floor 39A
(32.6-38.7 s/100m2/day)
Lu. intermedia s.l. ET forest floor 25A
(24 s/100m2/day)
Lu. pessoai ET 2A
Breeding places of phlebotomine sandflies
76 M. D. Feliciangeli

produced by the accessory glands (Dougherty et al., 1992) and Table 3. Summary of situations from which immature stages of
the response of gravid females to compounds emitted by faeces phlebotomine sandflies have been recovered
of chicken or rabbit (Dougherty et al., 1995), as well as to soil
Habitat Ectotope
bacteria isolated from natural breeding sites in India (Radjame
et al., 1997), support such a hypothesis. Domestic Abandoned buildings
Basements and cellars of houses
Tables 1–3 list the sites in domestic, peridomestic and
Cracks in mud floors and walls
silvatic habitats from which sandfly pre-imaginal stages
Soil in human dwellings
have sometimes been recovered. However, based on the Peridomestic Animal burrows
frequency of the collections and the abundance of speci- Animal shelters (cattle, pigs)
mens caught, only a few of them might be considered as Caves
stable breeding sites. Human dwellings and cattle sheds in Chicken coops
India and gerbil burrows in Central Asia (Perfil’ev, 1968) Debris and soil cracks
may be regarded as stable breeding sites of Phlebotomus Dry excreta of small domestic animals
papatasi. Developmental stages of P. duboscqi were Earth dyke
recovered from burrows of the giant African cane rat, Embankments
Cricetomys gambianus, by Dedet et al. (1982) and from
Rotted manure
unidentified rodent burrows in Kenya (Mutinga et al.,
Rubbish in the street
1986), Phlebotomus martini was found to breed mainly in Soil at the base of old walls
animal burrows, whereas termite hills were regarded as Under stones
secondary breeding sites in Kenya (Mutinga et al., 1989). Wells
Silvatic Ant nests
Burrows of gerbil and other rodents
Research on the breeding sites of sandfly Burrows of other animals (unknown)
vectors of leishmaniases Caves
Cesspits, dry
Studies on potential breeding sites of proven and suspected
vectors of leishmaniases are summarized in Table 1 for the
Hollow trees
Old World and Table 2 for the New World, in relation to Leaf litter on forest floor
the Leishmania parasites they transmit, the locality, meth- Nests of terrestrial tortoises
ods used and data on the work effort, if available. The Nests of birds
source of samples studied and the habitat (domestic, peri- Rocks, between and under
domestic or silvatic) are given. Results are expressed as the Roots of large trees
proportions of positive samples among those processed, the Soil at base of trees
amount of material screened and/or the numbers of positive Soil under overhanging rocks
and total emergence traps used. The number and stage(s) of Termite hills
specimens recovered (larvae or pupae) and the number of
species found are also reported with the source reference. Only two species of sandfly, P. argentipes in India and
For the known and suspected sandfly vectors of the P. chinensis in China, have been encountered repeatedly in
important leishmaniases (WHO, 1990), immature stages soil samples in the earth floor of human dwellings and cow-
have been recovered for at least 7 out of 10 proven vectors sheds, whereas only small proportions of the larvae and pupae
of Leishmania donovani s.l and Le. infantum in the Old of P. martini in Kenya have been found in the houses. Mutinga
World, as follows with their references: P. argentipes (Shortt & Kamau (1986) and Mutinga et al. (1989) stated that the main
et al., 1930, 1936; Smith et al., 1936; Pandya & Niyogi, 1980; breeding sites of this species are animal burrows and termite
Dhiman et al., 1983; Ghosh & Bhatthacharya, 1991), P. celiae hills, which serve as incubators with well regulated internal
and P. martini (Mutinga & Kamau, 1986; Mutinga et al., environments. Of the closely related P. celiae in Kenya, they
1989), P. ariasi (Killick-Kendrick, 1987), P. perfilievi and found only two males (from a tree-hole and a termite hill),
P. perniciosus (Pozio et al., 1980; Bettini et al., 1986; Bettini insufficient to reveal much about the breeding sites of this
& Melis, 1988) and P. langeroni (Doha et al., 1990). species. In southern Ethiopia, however, Leishmania-infected
Immature stages of P. tobbi, suspected vector of P. martini and P. celiae have been recovered from termite
Le. infantum around the eastern Mediterranean and Sicily, hills, suggesting that termite galleries may provide an import-
were detected in wells on the island of Zakinthos, Greece ant ecotope for the epidemiology of Le. donovani, the aetio-
(Biocca & Costantini, 1986). According to Professor Yan logical agent of kala-azar (Gebre-Michael & Lane, 1996).
Jia Leng (personal communication), larvae and pupae of Poor results were obtained from searching for the breed-
P. chinensis have been detected in several ecotopes (Table 1) ing sites of P. ariasi in the Cévennes focus of Leishmania
during extensive work on leishmaniasis and its vectors by infantum, causing canine and human visceral leishmaniasis
the East China Branch of the Chinese Academy of Medical in France. However, Killick-Kendrick (1987) reached the
Sciences (ECB/CAMS) and the East China Kala-azar conclusion that the larval ecotopes of P. ariasi are probably
Institute (ECKI). 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 77

The findings of Bettini (1989) in Sardinia were, as he vector of American visceral leishmaniasis, recovered by
wrote, ‘surely exceptional’. An abandoned cement structure Deane & Deane (1957) from animal corrals and among
(area 25 m2), used as a sheep shelter, was found to be rocks in Brazil. Those workers stressed the discrepancy
productive of three species of sandfly: Sergentomyia minuta between the abundance of Lu. longipalpis adult sandflies,
and two species of Phlebotomus (Bettini et al., 1986). After which they said were ‘found everywhere’ in the State of
sealing the shelter, they collected totals of 23 338 P. perfi- Ceará, Brazil, and the rarity of finding the pre-imaginal
liewi and 1309 P. perniciosus with six exit traps during 1983– stages. Similar results were obtained 40 years later
1985 (Bettini, 1989). Analysis of the substrate soil for tex- in Colombia, where more immatures were recovered from
ture, pH, CaCO3, organic matter and water content animal sheds close to houses rather than from isolated
showed no correlation with the number of sandflies that microhabitats (Ferro et al., 1997). No information is
emerged from the spots where soil samples were taken. available on the breeding sites of Lu. evansi, a proven vector
Apparently the developmental stages were associated of Leishmania infantum chagasi in Colombia (Travi et al.,
with a relatively stable, cool and humid environment pro- 1990) and Venezuela (Feliciangeli et al., 1999).
tected from sunshine and rain, rich in clay and organic In undisturbed Neotropical forests, where vector sand-
nitrogen. Sampling from a similar site in Tuscany, however, flies are closely associated with the wild animal reservoirs of
yielded very few specimens of these species (Pozio et al., Leishmania spp., pre-imaginal stages have been obtained for
1980). Immature stages of P. langeroni were found in Egypt 10 out of 42 proven or suspected vectors of cutaneous
(Doha et al., 1990), mainly in rubbish from stone piles. leishmaniasis (Killick-Kendrick, 1999). Notably, Lutzomyia
About the vectors of Le. tropica causing cutaneous gomezi, Lu. ovallesi, Lu. panamensis, Lu. trapidoi and Lu.
leishmaniasis, Mutinga & Odhiambo (1986) claimed that ylephiletor were all caught emerging from the forest floor in
P. guggisbergi breeds in Kenyan caves. In Romania, surveys Panamá (Hanson, 1968). Moreover, Rutledge & Ellenwood
of potential sandfly biotopes at Dobrudja, using oil papers, (1975a,b) pointed out that plant–sandfly interactions lar-
yielded only one P. sergenti (Nicolescu & Bı̂lbı̂e, 1980), gely determine the pattern of sandfly production in or on
although that species was formerly abundant in Canaraua the forest floor habitat; thus, Lu. trapidoi was associated
Fetii rocks (Duport et al., 1971). The decrease of P. sergenti with large lianas (Ouruparia and Sabicea), whereas
may be attributed to geological exploitation, spoiling the Lu. panamensis and Lu. gomezi were associated with large
sandfly breeding sites (Nicolescu & Bı̂lbı̂e, 1980). Anacardium trees. No plant association was established for
Regarding the most widespread form of cutaneous leish- Lu. ovallesi, although its larvae were found between tree
maniasis, caused by Leishmania major, the predominant buttresses (Hanson, 1968; Rutledge & Mosser, 1972). It was
vector Phlebotomus papatasi is well known and apparently inferred that Lu. ovallesi seeks out these sheltered places for
not complex (Parvizi et al., 2003): information on breeding oviposition, as adults seldom use these habitats for daytime
sites of this sandfly is available from several countries resting places (Rutledge & Ellenwood, 1975a,b). This beha-
(Table 1). In India, immature stages of P. papatasi have viour of Lu. ovallesi was also observed in north-central
been recovered consistently from cattle sheds and human Venezuela (Feliciangeli, 1987) where this species is the
dwellings in urban areas (McCombie-Young et al., 1926; main vector of cutaneous leishmaniasis (Feliciangeli &
Smith et al., 1936; Pandya & Niyogi, 1980; Dhiman et al., Rabinovich, 1998).
1983). In rural areas they have been found in various Arias & Freitas (1982) caught Lu. anduzei and Lu. umbra-
habitats: unused poultry houses made of bricks and clay, tilis, emerging from the ‘terra firme’ forest floor in the
manure heaps, caves, embankments, dried-up cesspits and central Amazon region of Brazil (Table 2). However, they
latrines (Sivagnaname & Amaldraj, 1997). In Egypt, breed- concluded that the open forest floor is not one of the major
ing sites of P. papatasi have been found in a similar range of breeding sites for these sandflies.
ecotopes (Artemiev et al., 1972; Doha et al., 1990). In the Breeding sites of Lu. whitmani and Lu. intermedia have
Central Asian Republics of the former Soviet Union, bur- been detected more often in the peridomestic than the
rows of the desert gerbil (Rhombomys opimus) are recog- silvatic habitat (Table 2), as demonstrated by Casanova
nized as breeding sites of this sandfly species (Perfil’ev, (2001) in rural areas of the Mogy Guaçu River, Brazil.
1968; Artemiev et al., 1972). Towards the equator, Dedet This tendency may be linked with changing epidemiological
et al. (1982) in Senegal and Mutinga et al. (1986) in Kenya patterns in the transmission of American cutaneous leish-
found P. duboscqi, the Afrotropical vector of L. major, maniasis (ACL), increasing risk factors being associated
breeding in animal burrows. with peri- and intradomiciliary habitats (Campbell-Lendrum
Caves were implicated as probable breeding sites of et al., 2001; Desjeux, 2001).
P. longipes and P. pedifer, proven vectors of Le. aethiopica,
studied by Foster (1972) in Ethiopia and by Mutinga &
Odhiambo (1986) in Kenya. Controlling the immature stages of phlebotomine
Far less is known about the breeding sites of phleboto- sandflies
mine sandfly vectors in the New World. Research on this
subject during a period of 20 years (1940–1960) yielded only This topic was reviewed by Alexander & Maroli (2003). For
60 specimens of immature phlebotomines (Hanson, 1961). eco-epidemiological reasons, it is important to focus on
Among these, 19 were Lutzomyia longipalpis s.l., the main 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 Medicine, U.K., for kindly providing photocopies of papers
phlebotomine sandflies, using necrocene with crude oil not available in Venezuela.
and kerosene mixture, was applied in India by Smith et al.
(1936), without much success. In the Central Asian Repub-
lics, destruction of burrows of the great gerbil (Psammomys)
effectively controlled P. papatasi (Faizulin et al., 1976), References
whereas chemical control with organochlorine insecticides
did not give such a good result (Vioukov, 1987). Larval Alexander, B. & Maroli, M. (2003) Control of phlebotomine
habitat modification by plastering walls of human dwellings sandflies. Medical and Veterinary Entomology, 17, 1–18.
and cattle sheds was quite effective to control P. argentipes, André, H.M., Ducarme, X. & Lebrun, P. (2002) Soil biodiversity:
the Indian vector of visceral leishmaniasis (Kumar et al., myth, reality or conning? Oikos, 96, 3–10.
Arias, J.R. & Freitas, R.A. (1982) On the vectors of cutaneous
1995). However, there were problems with the high cost of
leishmaniasis in the central Amazon of Brasil. 4. Sand fly
the product and its high viscosity, which made it difficult to emergence from a ‘terra firme’ forest floor. Acta Amazonica, 12,
spray. More encouragingly, selective application of the bio- 609–611.
pesticide Bacillus sphaericus (Bs) into the burrows of host Artemiev, M.M., Flerova, O.A. & Belyaev, A.E. (1972) Quantita-
rodents was successful against P. papatasi (Pener et al., tive evaluation of the productivity of breeding places of sandflies
1996). The Bs toxin works as a stomach poison against in the wild and in villages. Meditsinskaya Parazitologiya i
target insects, but it remains unclear whether the impact Parazitarnye Bolezni, 41, 31–35.
was mostly on immature or adult sandflies. Spraying plants Ashford, R.W. (2001) Phlebotomus fevers. The Encyclopedia of
with a sugar solution of B. sphaericus, for adult sandflies to Arthropod-Transmitted Infections (ed. by M. W. Service), pp.
ingest and carry back to poison the larvae, reduced sandfly 397–401. CABI Publishing, Wallingford, U.K.
Bettini, S. (1989) Sandfly breeding-sites. Life Sciences, 163,
populations emerging from animal burrows but not those
emerging from termitaria in Kenya (Robert et al., 1997). Bettini, S., Contini, C., Atzeni, M.C. & Tocco, G. (1986)
As no stable silvatic breeding sites of ACL vectors have Leishmaniasis in Sardinia. I. Observations on a larval breeding
yet been identified in the Americas, it remains impossible to site of Phlebotomus perniciosus, Phlebotomus perfiliewi perfiliewi
target the immature stages or to attempt sandfly source and Sergentomyia minuta (Diptera: Psychodidae) in the canine
reduction. Even so, some efforts to reduce sandfly popula- leishmaniasis focus of Soleminis (Cagliari). Annals of Tropical
tions were applied to tree-holes where they might affect Medicine and Parasitology, 80, 307–315.
immature as well as adult sandflies (Floch, 1957; Chaniotis Bettini, S. & Melis, P. (1988) Leishmaniasis in Sardinia. III. Soil
et al., 1982; Ready et al., 1985). Perhaps entomopathogenic analysis of a breeding site of three species of sandflies. Medical
fungi could be used against sandfly immatures in defined and Veterinary Entomology, 2, 67–71.
Biocca, E. & Costantini, R. (1986) I pozzi come possibili focolai
areas; for example Beauveria bassiana is applied to control
larvali di flebotomi nell’Isola de Zante. Annali dell’Istituto
the coffee berry borer Hypothenemus hampei in Colombian Superiore di Sanitá, 22, 59–60.
coffee plantations. Unfortunately, a trial evaluation of Birtles, R.J. (2001) Carrión’s disease. The Encyclopedia of
B. bassiana was unsuccessful for sandfly control (Reithinger Arthropod-Transmitted Infections (ed. by M. W. Service),
et al., 1997). Because of the increasingly close human–vector pp. 104–106. CABI Publishing, Wallingford, U.K.
associations, giving rise to greater risks of Leishmania trans- Campbell-Lendrum, B., Dujardin, J.P., Martinez, E.,
mission (Dye, 1996), there is growing hope and scope for Feliciangeli, M.D., Perez, J.E., Passerat de Silans, L.N.M. &
identifying restricted peridomestic breeding sites of sand- Desjeux, P. (2001) Domestic and peridomestic transmission of
flies that might be amenable to control, by larviciding or American cutaneous leishmaniasis: changing epidemiological
environmental modification to eliminate the source. 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.
Acknowledgements Chaniotis, B.N., Parsons, R.E., Harla, H.J. & Correa, M. (1982)
A pilot study to control phlebotomine sand flies (Diptera:
This review is dedicated to Dr Lawrence Quate, who, in Psychodidae) in a neotropical rain forest. Journal of Medical
1964, processed 2500 kg of soil in Sudan to recover only a Entomology, 19, 1–5.
single larva of Sergentomyia africana (Quate, 1964). With Comer, J.A. & Tesh, R.B. (1991) Phlebotomine sand flies as vectors
the recent death of Dr Quate, we have lost one of the very of vesiculovirus: a review. Parassitologia, 33 (Suppl.), 143–150.
few expert taxonomists of the family Psychodidae. Deane, L. & Deane, M.P. (1957) Observações sôbre abrigos e
criadouros de flebótomos no Noroeste do Estado do Ceará.
I wish to thank Dr Philippe Desjeux for the encourage-
Revista Brasileira de Malariologia e Doenças Tropicais, 9,
ment to publish this review and his helpful criticisms, 225–246.
Professor Yan Jia Leng for kindly providing me informa- Dedet, J.P., Desjeux, P. & Derouin, F. (1982) Écologie d’un foyer
tion on the breeding sites of vectors of leishmaniases in de leishmaniose cutanée dans la región de Thiès (Sénégal,
China, Dr Michele Maroli of the Istituto Superiore di Afrique de l’Ouest. 4. Infestation spontanée et biologie de
Sanitá, Roma, Italia, and Sinead Fitzpatrick, postgraduate Phlebotomus duboscqi Neveu-Lemaire 1906. Bulletin de la Sociéte´
student at the London School of Hygiene and Tropical de Pathologie Exotique, 75, 588–589.

# 2004 The Royal Entomological Society, Medical and Veterinary Entomology, 18, 71–80
Breeding places of phlebotomine sandflies 79

Desjeux, P. (2001) The increase in risk factors for leishmaniasis visceral leishmaniasis in the Aba Roba focus, southern Ethiopia.
worldwide. Transactions of the Royal Society of Tropical Medical and Veterinary Entomology, 10, 53–62.
Medicine and Hygiene, 95, 239–243. Ghosh, K.N. & Bhatthacharya, A. (1991) Breeding places of
Dhiman, R.C., Shetty, P.S. & Dhanda, V. (1983) Breeding habitats Phlebotomus argentipes Annandale and Brunetti (Diptera:
of phlebotomine sandflies in Bihar, India. Indian Journal of Psychodidae) in West Bengal. India Parassitologia, 33 (Suppl,
Medicine Research, 77, 29–32. 1), 267–272.
Doha, S., Kamal, H., Shehata, M., Helmy, N., Kader, M.A., El Said, Grassi, B. (1907) Ricerche sui flebótomi. Memorie della Societá
S. & El Sawaf, B.M. (1990) The breeding habitats of Phlebotomus Italiana di Scienze Naturali, 14, 353–394.
sand flies (Diptera: Psychodidae) in El Agamy, Alexandria, Egypt. Hanson, W.J. (1961) The breeding places of Phlebotomus in
Journal of the Egyptian Society of Parasitology, 20, 747–752. Panama (Diptera: Psychodidae). Annals of the Entomological
Dougherty, M.J., Guerin, P.M. & Ward, R.D. (1995) Identification Society of America, 54, 317–322.
on oviposition attractants for the sandfly Lutzomyia longipalpis Hanson, W.J. (1968) The immature stages of the family Phleboto-
(Diptera: Psychodidae) in volatiles of faeces from vertebrates. minae in Panama (Diptera: Psychodidae). PhD Thesis,
Physiological Entomology, 2, 23–32. University of Kansas, U.S.A.
Dougherty, M.J., Ward, R.D. & Hamilton, G. (1992) Evidence for Howlett, M. (1913) The breeding places of Phlebotomus. Journal of
the accessory glands as the site of production of the oviposition Tropical Medicine and Hygiene, 16, 255–256.
attractant and /or stimulant of Lutzomyia longipalpis (Diptera: Killick-Kendrick, R. (1987) Breeding places of Phlebotomus ariasi
Psychodidae). Journal of Chemical Ecology, 18, 1165–1175. in the Cévennes focus of leishmaniasis in the South of France.
Duport, M., Lupascu, G. & Cristescu, A. (1971) Contributions à Parassitologia, 29, 181–191.
l’étude des phlebotomes des biotopes naturels en Roumanie. Killick-Kendrick, R. (1990) Phlebotomine vectors of the leishma-
Archives Roumaines de Pathologie Expérimentales et Microbio- niases: a review. Medical and Veterinary Entomology, 4, 1–24.
logie, 30, 387. Killick-Kendrick, R. (1999) The biology and control of phleboto-
Dye, C. (1996) The logic of visceral leishmaniasis control. American mine sand flies. Clinics in Dermatology, 17, 279–289.
Journal of Tropical Medicine and Hygiene, 55, 125–130. King, H.H. (1913) Notes on the bionomics of the sandflies
El Naiem, D.A. & Ward, R.D. (1992) Oviposition attractants and (Phlebotomus) of Tokar, Anglo-Egyptian Sudan. Bulletin of
stimulants for the sandfly Lutzomyia longipalpis (Diptera: Entomological Research, 4, 83–84.
Psychodidae). Journal of Medical Entomology, 29, 5–12. King, H.H. (1914) Observations on the breeding places of sandflies
Faizulin, F.G., Kon’shina, L.N., Ummatov, A.M. & Abdullaev, (Phlebotomus spp.) in the Anglo-Egyptian Sudan. Journal of
I.V. (1976) The ploughing-up of burrows of the great gerbil as a Tropical Medicine and Hygiene, 17, 2–3.
method of controlling phlebotomines in the Golodnaya Steppe Kumar, V., Kesari, S.K., Sinha, N.K., Palit, A., Ranjan, A.,
natural focus of cutaneous leishmaniasis in the UzbekSSR. Kishore, K., Saran, R. & Kar, S.K. (1995) Field trial of an
Meditsinskaya Protozoologiya, 45, 104–105 (in Russian). ecological approach for the control of Phlebotomus argentipes
Feliciangeli, M.D. (1987) Ecology of sand flies (Diptera: Psycho- using mud and lime plaster. Indian Journal of Medical Research,
didae) in a restricted focus of cutaneous leishmaniasis in 101, 154–156.
northern Venezuela. II. Species composition in relation to MacFadyen, A. (1961) Improved funnel-type extractors for soil
habitat, catching method and hour of catching. Memorias do arthropods. Journal of Animal Ecology, 30, 171–184.
Instituto Oswaldo Cruz, 82, 125–131. Marrett, P.J. (1910) Preliminary report on the investigation into the
Feliciangeli, M.D. & Rabinovich, J. (1998) Abundance of Lutzomia breeding places of the sandfly in Malta. Journal of the Royal
ovallesi but not Lu. gomezi correlated with cutaneous leishma- Army Medical Corps, 15, 286–291.
niasis incidence in north-central Venezuela. Medical and Marrett, P.J. (1913) The Phlebotomus flies of the Maltese Islands.
Veterinary Entomology, 12, 121–131. Journal of the Royal Army Medical Corps, 20, 162–171.
Feliciangeli, M.D., Rodrı́guez, N., De Guglielmo, Z. & Rodrı́guez, A. Marrett, P.J. (1915) The bionomics of the Maltese Phlebotomi.
(1999) The re-emergence of American visceral leishmaniasis British Medical Journal, 1915, 172–173.
in an old focus in Venezuela. II. Vectors and parasites. Parasite, McCombie-Young, T.C., Richmond, A.E. & Brendish, G.R. (1926)
6, 113–120. Sandflies and sandfly fever in the Peshawar District. Indian
Ferreira, L.C., Deane, L. & Mangabeira, F.O. (1938) Sôbre a Journal of Medical Research, 13, 961–1021.
biologia dos flebótomos das zonas de leishmaniosis visceral ora Mitter, J.L. (1919) Preliminary report on an investigation into the
em estudo no Estado de Pará. O’Hospital, 14, 3–6. breeding places of Phlebotomus (papatasi and minutus) in
Ferro, C., Pardo, R., Torres, M. & Morrison, A. (1997) Larval Lahore. Indian Journal of Medical Research, 6, 452–61.
microhabitats of Lutzomyia longipalpis (Diptera: Psychodidae) Morsy, T., Aboul, R., Sarwat, M., Arafa, M. & El Gozamy, B.
in an endemic focus of visceral leishmaniasis in Colombia. (1993) Some aspects of Phlebotomus papatasi (Scopoli) in greater
Journal of Medical Entomology, 34, 719–728. Cairo, Egypt. Journal of the Egyptian Society of Parasitology, 23,
Floch, H. (1957) Sur la prophylaxie de la leishmaniose forestière 399–417.
américaine. Rivista di Malariologia, 36, 243–253. Mutinga, M.J. (1996) Phlebotomine sandflies (Diptera: Psychodi-
Forattini, O.P. (1954) Algunas observaçoes sobre a biologia dos dae): their importance and some aspects of control. East African
flebótomos dos zones de leishmaniose visceral ora em estudo do Medical Journal, 73, 48–49.
Estado de Para. O’Hospital (Rio de Janeiro), 14, 3–6. Mutinga, M.J. & Kamau, C.C. (1986) Investigations of the
Foster, W.A. (1972) Studies on Leishmaniasis in Ethiopia. III. epidemiology of Leishmaniasis in Kenya-II. The breeding-sites
Resting and breeding-sites, flight behaviour and seasonal of phlebotomine sandflies in Marigat, Baringo District, Kenya.
abundance of Phlebotomus longipes (Diptera: Psychodidae). Insect Science and its Applications, 7, 37–44.
Annals of Tropical Medicine and Parasitology, 66, 313–328. Mutinga, M.J., Kamau, C.C. & Kyai, F.M. (1986) Epidemiology
Gebre-Michael, T. & Lane, R.P. (1996) The roles of Phlebotomus of leishmaniases in Kenya. IV. Breeding habitats of Phlebotomus
martini and P. celiae (Diptera: Phlebotominae) as vectors of duboscqi (Diptera: Psychodidae), a vector of Leishmania major in

# 2004 The Royal Entomological Society, Medical and Veterinary Entomology, 18, 71–80
80 M. D. Feliciangeli

Marigat, Baringo District, Kenia. Insect Science and its Rutledge, L.C. & Ellenwood, D.A. (1975a) Production of
Applications, 7, 727–729. phlebotomine sandflies on the open forest floor in Panama:
Mutinga, M.J., Kamau, C.C, Kyai, F.M. & Omogo, D.M. (1989) the species complement. Environmental Entomology, 4, 71–77.
Epidemiology of Leishmaniases in Kenya. V. Wider search for Rutledge, L.C. & Ellenwood, D.A. (1975b) Production of
breeding habitats of phlebotomine sandflies in three kala-azar phlebotomine sandflies on the open forest floor in Panama:
endemic foci. East African Medical Journal, 66, 173–182. phitologic and edaphic relations. Environmental Entomology, 4,
Mutinga, M.J. & Odhiambo, T.R. (1986) Cutaneous leishmaniasis 83–89.
in Kenya. III. The breeding and resting sites of P. pedifer Rutledge, L.C. & Ellenwood, D.A. (1975c) Production of
(Diptera, Phlebotominae) in Mount Elgon focus, Kenya. Insect phlebotomine sandflies on the open forest floor in Panama:
Science and its Applications, 7, 175–180. hydrologic and phisiographic relations. Environmental Entomol-
Newstead, R. (1912) The papataci flies (Phlebotomus) of the ogy, 4, 78–82.
Maltese Islands. Bulletin of Entomological Research, 2, 47–78. Rutledge, L.C. & Mosser, H.L. (1972) Biology of immature
Nicolescu, G. & Bı̂lbı̂e, I.I. (1980) The scrutiny of phlebotomine sandflies (Diptera: Psychodidae) at the bases of trees in Panama.
sand flies (Diptera: Psychodidae) presence in natural biotopes in Environmental Entomology, 1, 300–309.
Dobrudja. Archives Roumaines de Pathologie Expérimentales et Seyedi Rashti, M.A. & Nadim, A. (1972) The use of Macfadyen’s
Microbiologie, 3, 271–281. technique for the collection of sand-fly larvae. Bulletin de la
Pandya, A.P. & Niyogi, A.K. (1980) Ecological study on immature Socie´te´ de Pathologie Exotique, 63, 881–884.
stages of phlebotomid sandflies in Gujarat. Indian Journal of Shortt, H.E., Smith, R.O.A. & Swaminath, C.S. (1930) The
Medical Research, 72, 355–358. breeding in nature of Phlebotomus argentipes Ann. & Brun.
Parvizi, P., Benlarbi, M. & Ready, P.D. (2003) Mitochondrial and Bulletin of Entomological Research, 21, 269–271.
Wolbachia markers for the sandfly Phlebotomus papatasi: little Shortt, H.E., Smith, R.O.A. & Swaminath, C.S. (1932) Miscellan-
population differentiation between peridomestic sites and gerbil eous experiments with Phlebotomus argentipes in relation to
burrows in Isfahan province, Iran. Medical and Veterinary transmission of kala-azar. Indian Medical Research Memoirs, 25,
Entomology, 17, 351–362. 90–102.
Penner, H. & Wilamowsky, A. (1996) Susceptibility of larvae of Sivagnaname, N. & Amaldraj, D.D. (1997) Breeding habitats of
the sandfly, Phlebotomus papatasi (Diptera: Psychodidae), vector sandflies and their control in India. Journal of Commu-
to Bacillus sphaericus. Bulletin of Entomological Research, 86, nicable Diseases, 29, 153–159.
173–175. Smith, R.O.A., Mukerjee, S. & Lal, C. (1936) Bionomics of
Penny, N.D. & Arias, J.R. (1982) Insects of an Amazon Forest. P. argentipes. Part II. The breeding-sites of P. argentipes and an
Columbia University Press, New York. attempt to control these insects by anti-larval measures. Indian
Perfil’ev, P.P. (1968) Diptera. Phlebotomidae (Sandflies). Fauna of Journal of Medical Research, 24, 557–562.
USSR, 3. Israel Program for Scientific Translations, Jerusalem. Southwood, T.R.E. (1966) Ecological Methods with Particular
Petrishcheva, P.A. & Izyumskaya, N.G. (1941) On breeding places Reference to the Study of Insect Populations. Methuen, London.
of Phlebotomus in Sebastopol. Trudy Voenno-Meditsinskoi Travi, B.L., Velez, I.D., Brutus, L., Segura, I., Jaramillo, C. &
Akademium. S. Kirova, 25, 243–254 (in Russian with English Montoya, J. (1990) Lutzomyia evansi, an alternate vector of
summary). Abstract (1946). Review of Applied Entomology (B), Leishmania chagasi in a Colombian focus of visceral leishma-
34, 78. niasis. Transactions of the Royal Society of Tropical Medicine
Pifano, F. (1941) La leishmaniasis tegumentaria en el Estado and Hygiene, 84, 676–677.
Yaracuy, Venezuela. Gaceta Me´dica de Caracas, 48, 292–299. Vieria, V.P., Ferreira, A.L. & Falqueto, A. (1999) Pesquisa do
Pozio, E., Gradoni, L., Bonarelli, R., Squitterin, N., Bettini, S., criadouros de flebotomineos no ambiente peridomiciliar, em
Maroli, M. & Cochi, M. (1983) Indagini sui focolai dei flebotomi área endêmica de leishmaniose tegumentar (LT) no Estado do
in provincia de Grosseto. Atti XII Congresso Nazionale Italiano Espirito Santo. Revista da Sociadade Brasiliera de Medicine
di Entomologia, 2, 395–400. Tropical, 32(Suppl. 1), 31–32.
Quate, L. (1964) Phlebotomus sandflies of the Paloich area in the Sudan Villani, M.G. & Gould, F. (1986) Use of radiographs for
(Diptera: Psychodidae). Journal of Medical Entomology, 1, 213–268. movement analysis of the corn wireworm, Melanotus communis
Radjame, K., Srinivasan, R. & Dhanda, V. (1997) Oviposition (Coleoptera: Elateridae). Environmental Entomology, 15, 462–
response of phlebotomid sandfly Phlebotomus papatasi to soil 464.
bacteria isolated from natural breeding habitats. Indian Journal Villani, M.G., Wright, R.J., Consolie, F.L. & Preston-Wilsey, L.
of Experimental Biology, 35, 59–61. (1989) Use of radiography in soil insect research. Journal of
Ready, P.D., Arias, J.R. & Freitas, R.A. (1985) A pilot study to Biology Photography, 57, 3–10.
control Lutzomyia umbratilis (Diptera: Psychodidae) the major Vioukov, V.N. (1987) Control of transmission. The Leishmaniases
vector of Leishmania braziliensis guyanensis, in a periurban in Biology and Medicine, Vol. 2 (ed. by W. Peters and R. Killick-
rainforest of Manaus, Amazonas State, Brazil. Memorias do Kendrick), pp. 909–928. Academic Press, London.
Instituto Oswaldo Cruz, 80, 27–36. WHO (1990) Control of the Leishmaniases. Technical Report
Reithinger, R., Davies, C.R., Cadena, H. & Alexander, B. (1997) Series, 793. World Health Organization, Geneva.
Evaluation of the fungus Beauveria bassiana as a potential biological Wittingham, H.E. & Rook, A.F. (1923) Observations on the life-
control agent against phlebotomine sandflies in Colombian coffee history and bionomics of Phlebotomus papatasi. British Medical
plantations. Journal of Invertebrate Pathology, 70, 131–135. Journal, 3285, 1144–1151.
Robert, L.L., Perich, M.J., Schlein, Y., Jacobson, R.L., Wirtz, R.A.,
Lawyer, P.G & Githure, J.I. (1997) Phlebotomine sand fly control
using bait-fed adults to carry the larvicide Bacillus sphaericus to
the larval habitat. Journal of the American Mosquito Control
Association, 13, 140–144. Accepted 10 February 2004

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