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

REVIEW ARTICLE

Natural breeding places of phlebotomine sandflies


M. D. FELICIANGELI
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
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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
(unpubl.)
Shandong DS 54/2808 (2%) Variousz E þ – ECB/CAMS & ECKI 1954
(unpubl.)
Breeding places of phlebotomine sandflies

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


Suizhong – Nicolescu & Bilbie, 1980
73
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

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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

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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
75
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
Latrines
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
Drains
Studies on potential breeding sites of proven and suspected
Garbage
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)
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areas; for example Beauveria bassiana is applied to control
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Association, 13, 140–144. Accepted 10 February 2004

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