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Studies on the flight patterns of foraging sand flies

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Acta Tropica 120 (2011) 110–114

Contents lists available at ScienceDirect

Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica

Studies on the flight patterns of foraging sand flies

R. Faiman, O. Kirstein, A. Moncaz, H. Guetta, A. Warburg ∗
Department of Molecular Genetics and Microbiology, The Institute for Medical Research Israel-Canada, The Kuvin Centre for the Study of Infectious and Tropical Diseases,
The Hebrew University – Hadassah Medical School, The Hebrew University of Jerusalem, 91120, Israel

a r t i c l e i n f o a b s t r a c t

Article history: Phlebotomine sand flies transmit Leishmania parasites that cause leishmaniasis in humans. We report
Received 7 May 2011 experimental results that improve our understanding of how foraging sand flies proceed over flat or
Accepted 24 June 2011 sloping ground and how they negotiate vertical obstacles. Three rows of traps were suspended at different
Available online 2 July 2011
heights on a wire fence. Those just above ground level captured 87% of all flies, traps set at one meter
captured 11% while only 2% of the flies were captured in traps set two meters above ground. When
Key words:
traps were deployed on a vertical support wall, the mean catch per trap was much higher than for traps
Phlebotomine sand flies
suspended on the fence. Traps suspended just above ground level captured 57% of all flies, traps set at
Flight height
Vertical obstacles
one meter above ground captured 27% of the flies and even traps set at two meters captured 16% of
Sticky traps the flies. Although, most flies were still captured close to the ground, a higher percentage reached the
Leishmaniasis second and third rows of traps. Sticky traps on a vertical wall produced similar results with significantly
more flies alighting on the lower sections of the trap closest to the ground. On a vertical sand fly-proof
net the overall dispersal of the flies was more like on a wall than in open space. Traps suspended just
above ground level captured 49%, traps set at one meter above ground captured 36% and traps set at
two meters captured 15% of the flies. Following spraying of the net with deltamethrin (1%), fewer sand
flies were captured but the reduction was not statistically significant. Our conclusions are that being
small and frail, sand flies tend to fly close to the ground probably in order to avoid being swept away by
gusts of wind. When they encounter a vertical obstacle, they proceed upwards close to the obstacle with
intermittent stops. Therefore, insecticide-sprayed walls or vertical nets should be effective for controlling
sand flies approaching human habitation.
© 2011 Elsevier B.V. All rights reserved.

1. Introduction in short flights, presumably remaining close to the vertical surface.

Phlebotomine sand flies (Diptera: Psychodidae) transmit Leish-
mania (Kinetoplastida: Trypanosomatidae) parasites that cause
cutaneous and visceral leishmaniasis (CL & VL) in tropical, subtrop-
ical and temperate regions of the World (Desjeux, 2004). Endemic
to Israel are three Leishmania species affecting humans. Leishmania
major, Yakimoff & Schokhor, 1914 and Leishmania tropica, Wright,
1903 cause CL while canine as well as rare cases of human VL, are
caused by Leishmania infantum Nicolle, 1908. Foci of both cutaneous
and visceral leishmaniasis are emerging in parts of the country hith-
erto free of the disease (Baneth et al., 1998; Jacobson et al., 2003;
Jaffe et al., 2004; Svobodova et al., 2006; Faiman et al., 2011).
Sand flies are small and frail insects that tend to advance in
short flights close to the ground, thereby avoiding winds as much
as possible (Killick-Kendrick, 1999). When sand flies encounter a
vertical barrier such as a wall or cliff, they may proceed upwards
∗ Corresponding author. Tel.: +972 26757080; fax: +972 26757425.
E-mail address: alonw@ekmd.huji.ac.il (A. Warburg).
Although there is no published evidence documenting this behav-
ior, cursory observations support its validity. In the central Jordan
Valley the predominant sand fly species is Phlebotomus (Phleboto-
mus) papatasi, Scopoli, 1786. Experiments were performed using
paper sheets smeared with castor oil to monitor the approach routs
of sand flies attracted to a commercial turkey pen. Turkey sheds
pens were surrounded by a 50 cm high solid cement wall above
which extended a chicken wire fence all the way up to the roof
(∼300 cm). Vertical columns of A4 paper sticky traps were posted
on the wall and mesh of the turkey shed beginning at different
heights above ground. An average of 38.5 flies (per 400 cm2 of
sticky surface) were captured in traps deployed over the wall and
up to 30 cm above it. Contrastingly, only 2.4 flies (per 400 cm2
of sticky surface) were captured between 80 and 220 cm above
ground (Warburg, unpublished). These results clearly demonstrate
that sand flies approaching and leaving the turkey sheds did so by
flying close to the ground and over the wall.
The behavioral trait observed in the described study, prompted
us to test the efficacy of vertical, insecticide-treated barriers for
intercepting phlebotomine sand flies approaching inhabited areas.

0001-706X/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.actatropica.2011.06.015
 Author's personal copy
R. Faiman et al. / Acta Tropica 120 (2011) 110–114
Fig. 1. Arrangement of un-baited suction traps in three rows:ground level, 1 m and 2 m above ground (staggered). A: traps set on diamond-wire fence, B: traps set on
supporting wall opposite the fence and below the peripheral houses, C: traps set on the fine mesh barrier (SpiderNet® 1240 holes/in.2 ) draped over the peripheral fence.
Studies were conducted in two separate CL foci; the first one
was in the town of Ma’ale Adumim, where L. tropica is trans-
mitted by Ph. (Paraphlebotomus) sergenti Parrot, 1917 and the
reservoir hosts are rock hyraxes (Procavia capensis Pallas, 1766)
(Orshan et al., 2010; Schnur et al., 2004; Talmi-Frank et al.,
2010). The second trial was conducted in Sde Eliyahu, an emerg-
ing focus of CL caused by L. major transmitted by Ph. papatasi
(Faiman et al., 2011).
In order to test means for protecting residents of affected neigh-
borhoods of Ma’ale Adumim from sand fly bites and CL, a 60 m long,
2 m high deltamethrin-impregnated net barrier (black polyester
barrier netting, 225 holes/in2. Vestergaard - Frandsen, Kolding,
Denmark) was erected to intercept sand flies approaching houses
from their natural habitats. The mean number of sand flies captured
with CO2 -baited CDC traps, behind the net barrier dropped by 60%
compared with untreated areas adjacent to the net. Importantly,
this effect was maintained even a year later after insecticide levels
in the net had dropped markedly (Faiman et al., 2009b). A some-
what larger scale experiment was conducted in Sde Eliyahu where
a 400 m long section of the peripheral fence of was draped with
a deltamethrin-impregnated net. Sand fly numbers collected near
houses behind the barrier decreased by 84.9% once the barrier was
in place (Faiman et al., in press).
The studies reported here were conducted in order to improve
our understanding of how sand flies negotiate vertical obstacles in
general and mesh barriers, with and without insecticide, in par-
ticular. Improved understanding of such behavior patterns should
facilitate our ability to devise effective and cost-efficient sand fly
control measures.
2. Materials and methods
2.1. Study sites
The town of Ma’ale Adumim (pop. 32,000) is situated approx-
imately 10 km east of Jerusalem in the Judean Desert (31◦ 47 N,
35◦ 18 E,: Altitude 400 m). Annual rainfall averages 200–400 mm,
summers are hot and winters are mild (Goldreich, 1998). The
studies described were performed on the perimeter fence below
Sheizaf street in the southern neighborhood of Tsemach Ha’sade.
The neighborhood is built on top of a ridge surrounded on three
sides with barren slopes growing sparse vegetation. In previous
studies using dyed sugar baits, (Schlein, 1987) flies were shown to
advance from the slopes towards the houses (Faiman et al., 2009b).
111
Kfar Adumim (31◦ 49 N, 35◦ 20 E,: Altitude 350 m) is an Israeli
village, (pop. ∼ 2500) in the Judean desert situated some 6 km to the
North East of Ma’ale Adumim. The climate is very similar to Ma’ale
Adumim although it is slightly warmer and there is slightly less
rainfall. Several studies on phlebotomine sand flies and cutaneous
leishmaniasis have been conducted in Kfar Adumim over recent
years (Orshan et al., 2010; Schnur et al., 2004).
2.2. Sand fly monitoring using suction traps
Sand flies in Ma’ale Adumim were trapped using un-baited CDC-
type traps assembled in our lab using parts identical to those used
by commercial manufacturers. Traps, powered by 6-volt recharge-
able lead-acid batteries (Model 3FM12, Amit Industries LTD.
Ashdod, Israel), were deployed in an updraft orientation Faiman
et al., 2009a) at different heights along a diamond-wire fence, stone
wall or net barrier (SpiderNet® 1240 holes/in.2 , Kleiman-Meteor,
Petah-Tikva, Israel, Fig. 1).
2.3. Sand fly monitoring using sticky traps
White polypropylene structured sheets (2.5 mm thick,
120 × 80 cm, Polygal, Ramat Hashofet, Israel) were affixed on
a supporting wall below houses of a street in Kfar Adumim in the
following arrangement. Two boards were pinned to the wall with
their long lower edge 50 cm above ground. These boards covered a
240 cm wide and 80 cm high section of the wall (50–130 cm above
ground). A further two boards were attached 130–210 cm above
ground. One of these boards was directly above the lower row
while the other protruded to the side in such a way that below
it was a non-sticky surface. The 3rd row of boards was similarly
placed partially above the 2nd covering a 240 cm wide section of
the wall at 210–290 cm above ground. The total sticky area of the
trap was 5.76 m2 (Fig. 2)
2.4. Sand fly identification
Sand flies trapped in suction traps were transported live or
on dry ice to the laboratory where they were counted, sexed
and preserved in 70% ethanol or frozen at −70 ◦ C. Sand flies
trapped on sticky surfaces were removed from the traps in the
field using pointed forceps and placed in dilute detergent solu-
tion to remove oil. In the lab, flies were washed and transferred
to 70% EtOH. Representative samples were dissected and mounted
 Author's personal copy

112 R. Faiman et al. / Acta Tropica 120 (2011) 110–114

Fig. 2. Sticky traps arranged at three levels on a vertical support wall: 50–130 cm, 130–210 cm and 210–290 cm. Each level comprised two boards measuring 120 × 80 cm
each (1.92 m2 ). Numbers depict average percentage of flies captured per 40 × 120 cm (0.48 m2 ) of the sticky surface. Total area of the sticky trap was 5.76 m2 .

in Hoyer’s medium on microscope slides for taxonomic identifi-
cation. Species were identified based on the morphology of the
external genitalia of males and the pharynx and spermathecae of
females, using several keys (Artemiev, 1978; Lewis, 1982; Perfil’ev,
1968).
2.5. Data analysis
Sand fly numbers were log-transformed [log (n + 1)] to normal-
ize the distribution and reduce the variance where non-normal
distribution, caused chiefly by multiform distribution was appar-
ent. This permitted the derivation of the geometric ‘Williams means’
(Mw), which presented a more accurate and sensitive mean than
the arithmetic mean and enabled the application of parametric
tests (Alexander, 2000; Bidlingmayer, 1985; Williams, 1937). To
determine whether parametric tests were appropriate, the distri-
bution and variance of the sand fly catch data were tested using
tests of normality; 1-Sample Kolmogorov–Smirnov Z test (K–S) for
raw trapping data, and Shapiro–Wilk’s test (S–W) for transformed
data and group means.
Univariate ANOVA was used to analyze the variance between the
groups of traps set at three different heights above ground or sand
fly yields at different locations on the sticky sheets. Fisher’s least
significant difference (LSD) post hoc test was used to analyze the
difference between trap groups or sheet locations once a significant
difference was obtained by ANOVA. All statistical analyses were
performed using SPSS Inc. statistical software for Windows® , ver-
sion 18 (PASW Statistics 18, IBM Corporation Inc.), and Microsoft®
Office Excel 2003/7.
3. Results
3.1. Sand fly species identification
A sample of 150 randomly-selected sand flies from Ma’ale Adu-
mim were identified and shown to comprise four species; 86% P.
sergenti, 6% P. papatasi, 4% P. syriacus and 4% P. tobbi. The flies on
sticky traps from Kfar Adumim comprised 70% Ph. sergenti, 30% Ph.
papatasi with very few unidentified Phlebotomus spp. In both loca-
tions numerous Sergentomyia spp were also collected but were not
included in the results.
3.2. Height of flight in open spaces
In the first experiment, three rows of traps were suspended
at different heights on a wire fence (diamond-shaped holes
dimensions 6 × 6 cm, Fig. 1A). Such a fence does not com-
prise an obstacle for flies that travel right through it. There
were eight traps per row and the experiment was repeated
for over nine nights. Traps suspended just above ground level
captured 87% of all flies [Mean ± SE/trap = 1.45(±0.26)]. Traps
set at one meter above ground captured only 11% of the flies
[Mean ± SE/trap = 0.19(±0.08]). Traps set at two meters captured
only 2% of the flies [Mean ± SE/trap 0.04(±0.03)] flies per trap
(Fig. 3). Although averages were generally very low because
the traps were not baited and were used without light, it
was quite clear that the absolute majority of sand flies tend
to stay – close to the ground (univariate ANOVAdf = 2 ; F = 37.8,
P < 0.05).
3.3. Behavior on vertical plain
In this experiment traps were set on a vertical support wall
below inhabited houses (Fig. 1B). The experiment was con-
ducted during five nights with eight traps per row. The mean
catch per trap was much higher than for traps suspended
on the fence. Traps suspended just above ground level cap-
tured only 57% of all flies [Mean ± SE/trap = 9.60(±1.40)]. Traps
set at one meter above ground captured 27% of the flies
[Mean ± SE/trap = 4.55(±0.55)]. Even traps set at two meters cap-
tured 16% of the flies [Mean ± SE/trap 2.66(±0.45)] (Fig. 4).
Although in comparison with the fence, a larger percentage of the
flies was captured by the second and third rows of traps, here too
the majority of the flies were collected at the foot of the wall (uni-
variate ANOVAdf=2 ; F = 15.9, P < 0.05).
In complementary experiments using sticky surfaces on a ver-
tical wall (Fig. 2) similar results were obtained with significantly
more flies alighting on the lower sections of the trap than on
the higher ones (Fig. 5). Contrary to our expectations, apart from
the lower edge closest to the ground there were no significant
differences between the number of flies captured close to the
edge of the sticky surface and further away from it (Fig. 2). This
finding indicates that flies can make longer flights up along the
wall before landing. There is also an indication that they may
 Author's personal copy
R. Faiman et al. / Acta Tropica 120 (2011) 110–114
Fig. 3. Traps on-wire fence—Bars represent geometric means (±SEM) of sand fly
catches for eight un-baited suction traps suspended on the diamond-wire fence
over nine nights. Traps set at different heights; Bottom bar = ground level, middle
bar = 1 m, top bar = 2 m above ground. Means with different letters are significantly
different (a and b, LSD, P < 0.000. b and bc; LSD, P = 0.602). In this experiment 87% of
the flies were trapped at ground level. Eleven percent (11%) were captured 1 m above
ground and only 2% at 2 m above ground. General mean comparison: Univariate
ANOVAdf=2 ; F = 35.3, P < 0.000.
fly in different directions and not only directly up toward the
houses.
3.4. Behavior on vertical fine mesh barrier
Traps were set on a vertical fine mesh net (SpiderNet® ,
1240 holes/in.2 . Kleiman-Meteor Inc. Petah-Tikva, Israel) draped
over ten meters of the peripheral fence (Fig. 1C). The exper-
iment was conducted during 5 nights with 7 traps per row.
The overall behavior of the flies was more like their behavior
on a wall than in open space. However, catches were gener-
ally low due to seasonal and perhaps annual fluctuations in
sand fly numbers. Traps suspended just above ground level
captured only 49% of all flies [Mean ± SE/trap = 0.93(±0.29)].
Traps set at one meter above ground captured 36% of the
flies [Mean ± SE/trap = 0.68(±0.15)]. Even traps set at two meters
captured 15% of the flies [Mean ± SE/trap 0.29(±0.12)] (Fig. 6). Fol-
lowing spraying of the net with deltamethrin (1%), fewer sand flies
were captured on the net. However, since numbers were so low
overall, the net reduction was not statistically significant (univari-
ate ANOVAdf=2 ; F = 1.99, P = 0.161).
Fig. 4. Traps on vertical support wall—Bars represent geometric means (±SEM)
of the sand fly catches of eight un-baited suction traps over five nights. Bottom
bar = ground level, middle bar = 1 m, top bar = 2 m above ground. Means with differ-
ent letters are significantly different (a and b, LSD, P < 0.000. b and bc; LSD, P = 0.131).
Along the wall 57% of the total catch was trapped at ground level, with 27% and 16%
at 1 m and 2 m above ground respectively. General mean comparison: Univariate
ANOVAdf=2 ; F = 15.9, P < 0.000.
113
Fig. 5. Sticky traps on vertical support wall—Means (±SEM) sand fly catches per sec-
tion of sticky trap (0.96 m2 – 240 cm W × 40 cm H, total of six). The experiment was
repeated seven nights and significantly more flies were captured on the lower sec-
tion (a) than on any of the higher ones (a; LSD, P < 0.000) which were not significantly
different from each other (b; LSD, P > 0.1). General mean comparison: Univariate
ANOVAdf=2 ; F = 35.1, P < 0.000.
Fig. 6. Traps on vertical mesh barrier—Geometric means (±SEM) sand fly catches per
un-baited suction trap. Bottom bar = ground level, middle bar = 1 m above ground,
top bar = 2 m above ground. White bars represent seven traps over four nights
on non-treated mesh. Black bars represent the same setup over two nights with
deltamethrin 1% sprayed on the net. Forty nine percent (49%) of the flies were
captured at ground level, with 36% and 15% at 1 m and 2 m high respectively. Fol-
lowing treatment, the number of sand flies declined, albeit non-significantly with
50% trapped at ground level and 50% at 1 m above ground level. General mean
comparison: Univariate ANOVAdf=2 ; F = 35.1, P < 0.000.
4. Discussion
It is generally agreed that sand flies advance in short flights along
the ground and when they encounter a vertical barrier, they pro-
ceed upwards in short flights. Our experiments did not discern short
vs. long flights. However, results of trapped flies on wire mesh con-
firm that the majority of flies tended to stay low, flying close to the
ground. The vast majority of flies were collected at ground level
with occasional flies reaching one meter. Almost no sand flies were
collected at two meters above ground.
The very low mean catches even at ground level, should be taken
to reflect the fact that un-baited traps were used in the current
study and not lack of sand flies. In fact, CO2 -baited traps deployed
repeatedly on many occasions in the same locations, one and two
years previously, yielded means surpassing 60 sand flies per trap
per night (Faiman et al., 2009b).
Significantly more flies were captured on the solid supporting
wall than on the wire fence. We interpret this finding to reflect
that flies reaching a wall do not all fly directly up but tend to pro-
ceed laterally along the foot of the wall. Such behavior mode may
cause them to pass by more than one trap, thereby increasing their
chances of being caught. On the other hand, the wire fence does
 Author's personal copy
114 R. Faiman et al. / Acta Tropica 120 (2011) 110–114
not constitute a barrier of any type for the sand flies that proceed
through it en route to the houses above the support wall.
In all experiments, more flies were captured close to the ground
than higher up. However, in traps set on wall and on a sand fly proof
porous obstacle (fine-mesh net), a larger minority proportion of the
flies were captured higher up (Figs. 4–6). The experimental setup
using sticky traps was designed to determine whether flies pro-
ceed upward in short flights—in which case there would be higher
numbers close to the edge of the sticky surface regardless of its
height on the wall. However, the only segment that captured more
flies than other segments was the lowest one close to the ground
(Figs. 2 and 5). All the rest of the sections captured comparable
numbers indicating that sand flies probably proceed in different
directions and their flights vary in distances.
According to the data presented here, one would expect that
insecticide-impregnated nets would be far more effective at block-
ing sand flies than untreated nets. Flies were captured relatively
high on the net (Fig. 6) and conceivably also reached the top and
flew on. However, two separate experiments showed that verti-
cal net barriers maintain their efficacy even once insecticide levels
drop and are no longer effective (Faiman et al., 2009b; Faiman et al.,
2011. Perhaps flies on the vertical net sense chemo-tactic cues (e.g.
CO2 ) as arriving through the net rather than from above (as would
be the case with a vertical wall on a slope). If this is indeed the
case, flies probably continue attempting to cross through the net
and thus fail to climb up and pass over it.
Acknowledgements
This research was supported by a grant from the Deployed
War-Fighter Protection (DWFP) Research Program, funded by the
U.S. Department of Defence through the Armed Forces Pest Man-
agement Board (AFPMB). Additional funding provided by The
Israel Science Foundation (grant no. 135/08) and the Deutsche
Forschungsgemeinschaft (DFG): “Emergence of cutaneous leish-
maniasis in the Middle East: an investigation of L. tropica in The
Palestinian Authority and Israel” (grant no. SCHO 448/8-1).
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