Journal of Vector Ecology March 2011
S128
A sharp increase in the natural abundance of sand flies in Kfar Adummim, Israel
Laor Orshan
Laboratory of Entomology, Ministry of Health, Israel
ABSTRACT: Monitoring sand flies in the cutaneous leishmaniasis foci Kfar Adummim and Ma’ale Adummim from May to
October generally yielded several hundred specimens per CO2 baited trap. In the summer of 2009, a sharp rise in the number
of sand flies trapped was recorded in Kfar Adummim, while numbers were similar to previous years in Ma’ale Adummim;
approximately 4,000 specimens compared to about 400, with maximal catches of about 16,500 specimens in Kfar Adummim.
We postulate that the sharp increase in sand fly numbers is directly related to the intensive construction conducted which
enhanced sand fly breeding habitats. Journal of Vector Ecology 36 (Supplement 1): S128-S131. 2011.
Keyword Index: Phlebotomus, sand flies, Israel, sharp increase, cutaneous leishmaniasis.
INTRODUCTION
Cutaneous leishmaniasis is endemic in the Judean
Desert. Leishmania tropica, the causative agent of the
disease in the region, is transmitted locally by Phlebotomus
(Paraphlebotomus) sergenti Parrot (Jaffe et al. 2004, Schnur
et al. 2004). Since 2005, regular sand fly surveillance has
been carried out in the two adjacent endemic foci: the town
of Ma’ale Adummim and the village of Kfar Adummim.
Phlebotomus sergenti was predominant in outdoor
collections, comprising about 90%. Densities of several
hundred specimens per CO2 baited trap were common in
collections from May to October. No marked differences
were observed between the two locations and between
different years (Orshan et al. 2010).The present report
describes the dramatic increase in sand fly numbers in
the 2009 collections from Kfar Adummim compared with
past years and parallel collections from Ma’ale Adummim.
Possible explanations are discussed. MATERIALS AND METHODS
Study sites
The village of Kfar Adummim (population ~2,500, area
~7 km2, altitude ~350 m) and the town of Ma’ale Adummim
(population ~33,000, area ~50 km2, altitude 400-450 m) are
situated in the desert on the eastern slopes of the Judean
Hills, 6 km apart. The residential neighborhoods are
sprawled over the ridges and separated by deep uncultivated
valleys. The summer (May to October) is dry and hot with
day temperatures of 30° C, often reaching 40° C, and night
temperatures usually above 20° C. The rainy season is
between November and April, and the mean annual rainfall
is 150-250 mm.
In Kfar Adummim (Figure 1), large scale construction
began at the end of 2008. Deep trenches were dug for a new
sewer pipe system along the outer perimeter of the village,
and intensive construction work was carried out on the
western extension. During these activities, the upper layer of
the ground was disturbed, and the dugout earth was spread
over the natural slopes as loose dirt rockfalls (Figure 2). Sand fly collection
Sand fly densities were monitored in 2007-2009 at two
locations in Kfar Adummim (marked on Figure 1) and
four locations in Ma’ale Adummim. Traps were set at each
location during 2-4 nights each month between May and
November. Additional traps were set occasionally along the
whole length of the southeast-facing circumference road.
Suction traps were baited with dry ice and powered by two
1.2 V GP2700 AA rechargeable batteries. The traps were
placed in a vertical position, openings parallel to the ground
at a height of about 10 cm, with the fan causing updraft
airflow and collection boxes hanging above the body of the
trap. In September 2009, four non-baited suction traps were
operated over 4 nights in the two locations (i.e. total of 16
traps over 4 nights per location). The catches were brought
to the laboratory, chilled, sorted and counted. Males were
identified to species. In 2009, sand fly numbers in catches
exceeding ~1,000 specimens were estimated by weight. The
whole sample and sub-sample comprising several hundred
specimens were weighed. Sand fly numbers were counted
in the sub-sample, and the total catch was estimated by the
proportional weight of the sub-sample. Figure 1. Aerial photo of Kfar Adummim. Journal of Vector Ecology
Vol. 36, Supplement 1
Figure 2. Kfar Adummim, a view of the western extension
from the south. Calculations and statistics
The mean number of sand flies per trap night was
calculated for each location for each trapping season.
Significant differences between locations were tested with
an independent sample t-test. Mean numbers of sand flies
in different years for each location were analyzed with
ANOVA. SPSS 17.02 (SPSS, Chicago, IL) was used for all
statistical tests.
RESULTS
A total of 94,600 sand flies was collected from two
locations in Kfar Adummim using 82 traps in 41 nights and
87,465 from four location in Ma’ale Adummim using 204
traps in 51 nights. Phlebotomus sergenti was predominant
and comprised 98% of all collections in Kfar Adummim
and 96% in Ma’ale Adummim. The other species were
Phlebotomus (Phlebotomus) papatasi (Scopoli), Phlebotomus
(Larroussius) syriacus Adler & Theodor and Phlebotomus
(Larroussuis) tobbi Adler & Theodor (Table 1).
In 2007 and 2008, traps baited with dry ice caught
a mean (±SE) of 362 ± 47 (range = 100 - 1,421) and 405
± 49 (82 - 1,387) sand flies in Kfar Adummim and 396
± 20 (76 - 879) and 457 ± 32 (75 – 1,349) flies in Ma’ale
Adummim, respectively (Table 2). The minor differences
between the two locations were not statistically significant
(2007: t = -0.776, df = 124, p = 0.439; 2008: t = -0.903, df =
81, p = 0.348). Similar numbers (454 ± 34; 42 - 953), were
collected from Ma’ale Adummim throughout the summer
of 2009, while 6 km away in Kfar Adummim, a drastic
increase in sand fly densities was observed (Table 2, Figure
3). Numbers in traps increased from 582 ± 229 in May 2009
to a peak of 9727 ± 3983 in September 2009 with a maximal
yield of ~17,500 sand flies per trap. Despite the remarkable
differences in numbers collected in Kfar Adummim in
2009, gender proportion (1:1) and species composition (P.
sergenti comprising ~ 98%) were similar in all three years
(2007-2009) (proportion of females; F = 2.343, df = 2, p =
0.102; species composition F = 1.374, df = 2, p = 0.259). S129
Table 3 summarizes the trapping data of September
2009. Dry ice-baited traps placed in Kfar Adummim
collected 16 times more sand flies (9727 ± 3983) than
traps in Ma’ale Adummim (619 ± 69). Catches were much
smaller in non-baited traps: 241 ± 23 flies per trap in Kfar
Adummim and 14 ± 3 in Ma’ale Adummim. However, the
proportion between catches from the two locations with
non-baited traps (17:1) was similar to those obtained with
dry ice baited traps (16:1). Proportions between the catches
of dry ice-baited traps and non-baited traps in each location
were also similar. A proportion of 40:1 was noted in Kfar
Adummim and 44:1 in Ma’ale Adummim.
In the summer of 2009, several thousand sand flies or
a few hundred were collected with dry ice-baited traps and
non-baited traps, respectively, from each sampling location
along the southern circumferential road (length 1.5 km).
DISCUSSION
Phlebotomus sergenti, the local vector of L. tropica,
predominates in outdoor sand fly collections from the
Judean Desert cutaneous leishmaniasis foci, the village of
Kfar Adummim and the town of Ma’ale Adummim (Table 1,
Orshan et al. 2010). Collections from the two adjacent foci
were similar, and yields of several hundred specimens per
dry ice-baited trap were common throughout the summer
and autumn months of 2007 and 2008 (Table 2, Figure
3). A drastic change was observed in Kfar Adummim in
2009, when number of sand flies in traps increased from
hundreds to thousands per trap, representing a 16-fold
increase compared with catches in previous years and also
catches from Ma’ale Adummim (Table 2, Figure 3). Similar
difference in sand fly densities between Kfar Adummim
and Ma’ale Adummim were also observed with non-baited
traps (Table 3). The increase in numbers did not involve
a change in species composition in female:male ratio or
in Leishmania infection rates (Orshan et al., unpublished
data). Catches of similar size were seen in traps set
anywhere along the southern circumferential road, which
indicated that high densities of sand flies were widespread
and not focal. This phenomenon affected the entire village.
Residents complained about unusual burden of sand fly
bites in comparison with previous years. Inspection of
houses often revealed dozens of sand flies in a single room.
The accumulation of observations in Israel has led to
an association of complaints about the sudden increase in
nuisance biting sand flies with construction work in nearby
locations. This phenomenon has been observed in areas
characterized by the expansion of existing settlements and
houses adjacent to construction sites. In Jordan (Kamhawi
et al. 1991) and Morocco (Boussaa et al. 2007), it was
shown that the demolition and reconstruction of human
habitation initially decreased sand fly populations, but
later the populations recovered and expanded beyond
pre-construction levels. In such desert areas, low soil
humidity was considered to be the main factor limiting P.
papatasi breeding (Schlein et al. 1984, Wasserberg et al.
2003ab). It is suggested that the widespread construction
Journal of Vector Ecology March 2011
S130
Table 1. Summary of sand fly collections and species composition.
No. trap
nights
No.
collected
2007
32
2008
Location and year
Kfar Adummim
Ma’ale
Adummim
P. sergenti
males
Males
P. papatasi
males
P. syriacus
males
P. tobbi
males
No.
%
No.
%
No.
%
No.
%
No.
%
11,572
5,953
51.4
5,870
98.6
40
0.7
40
0.7
3
0.1
32
12,966
6,430
49.6
6,326
98.4
44
0.7
54
0.8
6
0.1
2009
18
70,062
35,168
50.2
34,511
98.1
617
1.8
22
0.1
18
0.1
Total
82
94,600
47,551
50.3
46,707
98.2
701
1.5
116
0.2
27
0.1
2007
92
36,419
18,651
51.2
18,069
96.9
253
1.4
314
1.7
15
0.1
2008
56
25,609
13,474
52.6
12,855
95.4
145
1.1
469
3.5
5
0.0
2009
56
25,437
12,879
50.6
12,143
94.3
208
1.6
469
3.6
59
0.5
Total
204
87,465
45,004
51.5
43,067
95.7
606
1.3
1,252
2.8
79
0.2
Table 2. Number of sand flies caught in dry ice-baited traps.
Year
Kfar Adummim1
Ma’ale Adummim2
2007
Mean ± SE (range)
2008
Mean ± SE (range)
2009
Mean ± SE (range)
362 ± 47a
(100 – 1,421)
396 ± 20a
(76 - 879)
405 ± 49b
(82-1,387)
457 ± 32b
(75 – 1,349)
3,892 ± 849c
(88 – 17,690)
454 ± 34c
(42 - 953)
Significant differences between years (ANOVA, df = 2, F = 15.304, p < 0.001).
No significant differences between years (ANOVA, df = 2, F = 1.864, p = 0.158).
a
No significant differences between locations (independent sample t-test, t = -0.776, df = 124, p = 0.439).
b
No significant differences between locations (independent sample t-test, t = -0.903, df = 81, p = 0.348).
c
Significant difference between locations (independent sample t-test, t = 3.086, df = 63, p=0.006).
1
Mean no./trap
2
Figure 3. Sand fly densities in Kfar Adummim and Ma’ale Adummim in the summer months of 2007-2009.
Vol. 36, Supplement 1
Journal of Vector Ecology
in Kfar Adummim and the groundcover representing
large areas with loose dirt rockfalls (Figure 2) increased
the absorption capacity of the area and the seepage of
water into deeper layers of the ground, thus enhancing the
development of suitable niches for sand fly breeding. If the
sharp increase in the number of sand flies is the result of
widespread construction, sand fly densities are expected
to decrease after the completion of the construction work
and subsequent ground stabilization. Sand fly monitoring
in the two locations will be continued. Possible ways to
prevent or reduce outbursts of sand fly populations using
environmental modification, such as soil compacting
during and after construction, will be examined.
Acknowledgments
The assistance of David Szekely in the field, Liora
Studentski in the laboratory and the technical assistance of
Tamar Yeger are acknowledged. This study was part of the
Israeli Government sand fly surveillance program.
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