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Diversity of sand flies (Diptera, Psychodidae) in southwest Iran with emphasis on synanthropy of Phlebotomus papatasi and P. alexandri
ARTICLE in ACTA TROPICA · AUGUST 2014 Impact Factor: 2.27 · DOI: 10.1016/j.actatropica.2014.08.017 · Source: PubMed
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Elham Jahanifard Yavar Rassi Tehran University of Medical Sciences Tehran University of Medical Sciences
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Mohammad Mehdi Sedaghat mohammad reza Shirzadi Tehran University of Medical Sciences Ministry of Health, Iran
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Available from: Yavar Rassi Retrieved on: 18 October 2015
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ACTROP 3445 1–8 ARTICLE IN PRESS
Acta Tropica xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Acta Tropica
jo urnal homepage: www.elsevier.com/locate/actatropica
1 Diversity of sand flies (Diptera, Psychodidae) in southwest Iran with
2 emphasis on synanthropy of Phlebotomus papatasi and Phlebotomus
3 alexandri
∗ ∗
4 Q2Q1 Elham Jahanifard, Mohammad Reza Yaghoobi-Ershadi , Amir Ahmad Akhavan ,
5 Kamran Akbarzadeh, Ahmad Ali Hanafi-Bojd, Yavar Rassi, Mohammad Mehdi Sedaghat,
1
6 Mohammad Reza Shirzadi , Ameneh Karimi
7 Department of Medical Entomology &Vector Control, School of Public Health, Tehran University of Medical Sciences, Enghlab Ave. Poorsina St. Tehran, PO
8 Box 6446, Tehran, Iran
9
2510 a r t i c l e i n f o a b s t r a c t
11
12 Article history: Zoonotic Cutaneous Leishmaniasis (ZCL) is still a serious health problem in Iran. The objective of the
13 Received 22 February 2014
study was to determine the differences in sand fly biodiversity in Shush (plain) and Khorramshahr (lit-
14 Received in revised form 12 August 2014
toral) Counties, Khuzestan Province, southwest Iran. Sand flies were collected using sticky paper traps
15 Accepted 18 August 2014
from urban, semi urban, agricultural and natural ecotypes. Alpha and beta diversity were calculated using
16 Available online xxx
Shannon–Weiner index and Jaccard’s and Sorensen’s coefficients, respectively. Synanthropic index was
17
determined for the first time for Phlebotomus papatasi and Phlebotomus alexandri in different land use
18 Keywords:
categories in Iran. Totally 11213 specimens, 68.47% in Shush and 31.53% in Khorramshahr, were col-
19 Diversity
lected. Eleven species of sand flies including, 2 of genus Phlebotomus and 9 of genus Sergentomyia were
20 Synanthropic index
21 Richness identified. Sergentomyia christophersi was found as a new record. Dominant species were P. papatasi and
22 Shannon–Weiner index Sergentomyia sintoni. Shannon–Weiner index, richness and evenness in semi urban area of Shush County
␣
23 Ecology of sand flies were more than other habitats. The analysis of biodiversity showed that agricultural ecosystem of Khor-
24 Iran ramshahr County had the highest diversity due to maximal richness and diversity and also relatively high
evenness. Comparison of similarity of the sand flies population composition between Shush and Khor-
ramshahr indicated the maximum similarity between the urban area of Shush and the semi urban area of
Khorramshahr (Sj = 75% and Ss = 86%). Synanthropic index of P. papatasi and P. alexandri were calculated
−
to be 83.34 and −91.18, respectively in Shush County. Estimated synanthropic indices for P. papatasi
and P. alexandri in three habitats (natural, semi urban and urban) habitats of Khorramshahr County were
−
69.84 and −85.89, in the same order. The factors for having high diversity of sand flies in the plain area
studied may be due to higher annual precipitation, the related land use and land cover. The changes on
the composition of sand flies are perhaps due to human intervention in their natural habitats.
© 2014 Published by Elsevier B.V.
26 1. Introduction (Yaghoobi-Ershadi, 2012). Khuzestan Province in Southwest Iran is 30
considered to be an important endemic focus of Zoonotic Cutaneous 31
27 Cutaneous Leishmaniasis (CL), due to Leishmania major is a Leishmaniasis (ZCL) due to environmental impact of the warfare 32
28 neglected disease that occurs throughout the old world. In Iran, (Nadim et al., 2008). In the past, the incidence of ZCL was relatively 33
29 disease is endemic in many rural areas of 17 out of 31 provinces low; however, as a result of high CL incidence among soldiers dur- 34
ing Iran–Iraq war, leishmanization program was carried out from 35
1982 to 1989 on more than 200,000 Iranian soldiers. During the war 36
(1980–1988), there were over 10,000 reported cases among sol- 37
∗
Corresponding authors. at: Department of Medical Entomology & Vector Control, diers and immigrants every year. In 1983, more than 3000 patients 38
School of Public Health, Tehran University of Medical Sciences, Tehran, Iran, P. O. were treated at health centers and clinics in Khuzestan (Nadim 39
Box 6446, Tehran 14155, Iran. Tel.: +0098 21 42933114; fax: +0098 21 88951393.
et al., 2008). 40
E-mail addresses: [email protected], [email protected]
The first entomological studies on CL in Khuzestan were con- 41
(M.R. Yaghoobi-Ershadi), [email protected] (A.A. Akhavan).
1 ducted during 1962 in Shush, Dezful, Abadan, Izeh and Ahvaz 42
Zoonoses Department, Center of Diseases Control (CDC), Ministry of Health and
Medical Education, Tehran, Iran. Counties and 20 sand fly species were collected: Phlebotomus 43
http://dx.doi.org/10.1016/j.actatropica.2014.08.017
0001-706X/© 2014 Published by Elsevier B.V.
Please cite this article in press as: Jahanifard, E., et al., Diversity of sand flies (Diptera, Psychodidae) in southwest Iran with emphasis on
synanthropy of Phlebotomus papatasi and Phlebotomus alexandri. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.08.017
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44 alexandri Sinton, Phlebotomus halepensis Theodor, Phlebotomus (1999) found that soil types and underlying geology can model the 110
45 jacusieli Theodor, Phlebotomus keshishiani Shchurenkova, Phle- distribution of sand flies in central and southern Sinai. 111
46 botomus neglectus Tonnoir, Phlebotomus mongolensis Sinton, Alpha (or within habitats) diversity is the most common form 112
47 Phlebotomus papatasi (Scopoli), Phlebotomus tobbi Adler, Theodor of inventory diversity, which records the number of taxa per area 113
48 & Lourie, Phlebotomus salehi Mesghali, Phlebotomus sergenti Par- of homogenous habitat therefore reflecting species packing within 114
49 rot, Sergentomyia antennata Newstead, Sergentomyia baghdadis a community. Beta (or between habitat) diversity is the category of 115
50 (Adler & Theodor), Sergentomyia dentata arpaklensis (Perfiliev), differentiation diversity that measures the variation in taxonomic 116
51 Sergentomyia iranica Lewis & Mesghali, Sergentomyia mervynae composition between areas of alpha diversity (Magurran, 1988). 117
52 Pringle, Sergentomyia palestinensis Adler & Theodor, Sergentomyia To obtain useful information about vector control and their bio- 118
53 sintoni Pringle, Sergentomyia squamipleuris (Newstead), Sergento- logical indicators of environmental changes caused by man, the 119
54 myia theodori Parrot and Sergentomyia tiberiadis Adler, Theodor & present study aimed to identify the current situation of species 120
55 Lourie (Nadim et al., 1974). Another study conducted in Ahvaz and composition, diversity, richness and community similarity of sand 121
56 Dezful also added two other species of Sergentomyia clydei Sinton flies and analyzing the level of synanthropy of species captured in 122
57 and Sergentomyia pawlowski Perfiliew to the sand flies fauna of this different ecotypes in two important foci of ZCL located in Khuzestan 123
58 province (Javadian and Nadim, 1975). Jahanifard et al. (2009) also Province, plain (Shush) and littoral (Khorramshahr) areas, which 124
59 reported P. papatasi, P. alexandri and P. mongolensis in Hoveizeh and experienced extensive environmental changes over the last three 125
60 Shadegan marshlands of Khuzestan. Natural promastigote infection decades. 126
61 was observed in several occasions in P. papatasi, P. alexandri and S.
62 sintoni from rodent burrows in Ahvaz, Shush and Shushtar Counties
63 (Javadian and Mesghali, 1974) of the province. Kavarizadeh et al. 2. Materials & methods 127
64 (2013) collected 10 species of sand flies (P. papatasi, P. alexandri, P.
65 mongolensis, S. sintoni, S. antennata, S. mervynae, S. theodori, S. clydei, 2.1. Study area 128
66 S. tiberiadis and S. palestinensis) in Musian District, situated in north-
67 west Khuzestan Province. Also, they reported species composition The study was conducted from March 2012 to January 2013 129
68 in Musian to be the same as those in other parts of Iran. in two counties of Khuzestan Province, Shush and Khorramshahr, 130
◦ ◦ ◦ ◦
69 Akhoundi et al. (2012) collected 16 species of sand flies (P. southwest Iran. Shush County (32 11 21 N, 48 15 28 E) is sit- 131
70 papatasi, P. sergenti, P. mongolensis, Phlebotomus caucasicus, Phle- uated in northwest of Khuzestan at an altitude of 71 m above 132
71 botomus jacusieli, Phlebotomus major s.l., P. tobbi, Phlebotomus the sea level (Fig. 1), with a hot and arid climate. In 2012, 133
72 perfiliewi, Phlebotomus kandelakii, P. halepensis, Phlebotomus bre- the average maximum and minimum monthly temperatures 134
◦
73 vis, Phlebotomus longiductus, Phlebotomus balcanicus, S. sintoni, S. were reported to be 15.9–30.23 C. The total annual rainfall 135
74 dentata and S. theodori in northwestern Iran in 2010. P. papatasi was 236.8 mm (https://edata.sci.org.ir/AllUser/Directory TreeCom- 136
75 had been the predominant species in many areas, followed by P. plete.aspx). Wheat, rice, corn and summer crops are the major 137
76 perfiliewi and P. kandelakii. They found that two districts (Meshkin- produces. The county has 3 districts, 5 towns and 195 villages. 138
◦ ◦ ◦ ◦
77 Shahr and Sarab) had the highest similarity with a high diversity Khorramshahr County (48 10 45 N, 30 26 21 E) at an altitude 139
78 and richness. of 3 m is located in the southwest of Khuzestan Province, and 140
79 P. papatasi is the main vector of L. major in Iran as it is being bounded on the west by Iraq and on the south by the Persian 141
80 collected from different provinces of the country with an altitude Gulf (Fig. 1). It has hot, long summers with mild, short win- 142
81 range of 8 to 1756 m (Yaghoobi-Ershadi, 2012). P. alexandri has also ters. The average minimum and maximum monthly temperatures 143
◦
82 been reported as a probable vector of Zoonotic Visceral Leishman- were 18.5 and 33.62 C, respectively. The total annual rainfall 144
83 iasis (ZVL) in Iran (Azizi et al., 2006). Furthermore, these species was 112.4 mm (https://edata.sci.org.ir/AllUser/Directory TreeCom- 145
84 together with Phlebotomus andrejevi, P. caucasicus, P. mongolen- plete.aspx). Khorramshahr experiences many sandstorms. Date and 146
85 sis and Phlebotomus ansarii are suggested to be the vectors of ZCL rice are the major crops in this county. The county has 2 districts, 2 147
86 among rodents in rural areas (Yaghoobi-Ershadi et al., 2005). Altitu- towns and 67 villages. It should also be mentioned that the province 148
87 dinal distribution of P. alexandri was reported from the sea level to of Khuzestan is a major natural oil and gas reservoir in Iran. Oil 149
88 1500 m (Maroli et al., 2001; Kamal et al., 2003). This species is gen- and gas development on public lands has contaminated soil, air, 150
89 erally distributed in mountainous regions although reported from water, damaged ecosystems, animal habitats, species biodiversity 151
90 almost all parts of Iran (Yaghoobi-Ershadi, 2012). Cutaneous leish- and their behavior. Furthermore, the presence of main the vector 152
91 maniasis became epidemic twice in Khorramshahr County during of ZCL, P. papatasi, and non-endemic workers facilitate preserving 153
92 1990–1991and 2009. It is a serious endemic health problem in the leishmaniasis in this Province. 154
93 Shsuh area (Institute of Public Health, unpublished data). For the purpose of this study, sampling was performed in four 155
94 Little data are available on the diversity, species composition, ecotypes (natural, agricultural, semi urban and urban) in each 156
95 and distribution of sand flies in different land use categories of county, where the cases of ZCL have been recorded. Six fixed places 157
96 Khorramshahr and Shush. Furthermore, data on leishmaniasis vec- were selected from each county. In order to maximize the oppor- 158
97 tors should be updated regularly in order to prepare the control tunity to catch sand flies from other locations, four random places 159
98 programs. Monitoring the insects in natural ecosystem is one of have been selected in each county. Six fixed collection areas in 160
99 the simplest ways to observe and provide early warning of changes Shush were natural (Shavoor and Malhe), agricultural (Aboozar 161
100 to biodiversity and habitat structure (Uribe-M et al., 2010). Synan- and Danesh), semi urban (Shahrak Salman) and urban (Zamin- 162
101 thropic species, associated with humans, are able to transmit shahri) while the fixed areas in Khorramshahr included: natural 163
102 pathogen either mechanically or biologically. On the other hand, (Arayez and Kofaysheh), agricultural (Menikh and Haneishyeh), 164
103 synanthropy indicates the degree of avoidance of human associa- semi urban (Sarhanyeh) and urban (Taleghani). JaryehSaydRazi, 165
104 tion (Das et al., 1981). Hanoosh, Shahrak Bahram and Ebrahimabad in Shush County and 166
105 Sand flies are very sensitive to environmental changes. In this Shaneh, Mino Island, Abareh, Sotongar in Khorramshahr County 167
106 regard, soil type, land use and modification of natural habitats are were selected at random for natural, agricultural, semi urban and 168
107 critical factors affecting changes in the vector, reservoir population urban habitats, respectively. By natural habitat, we mean an eco- 169
108 densities, and leishmaniasis risks (Yuval, 1991; Fryauff et al., 1993; logical or environmental area inhabited by a particular species of 170
109 Kassem et al., 1999; Hassan et al., 1999). Furthermore, Kassem et al. animal, plant or other type of organism. The agricultural habitat was 171
Please cite this article in press as: Jahanifard, E., et al., Diversity of sand flies (Diptera, Psychodidae) in southwest Iran with emphasis on
synanthropy of Phlebotomus papatasi and Phlebotomus alexandri. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.08.017
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Fig. 1. Map showing the study areas in Khuzestan Province, southwest Iran, 2012.
172 supposed to just have more agricultural land than natural habitat. species, by N, the total number of collected individuals (Magurran, 203
173 The urban area was considered for its higher population density and 2004). 204
174 the vast human features compared to the surrounding areas. Semi Evenness index (E) can be calculated by dividing H index by nat- 205
175 urban areas differ from rural and urban areas in terms of configura- ural logarithm (ln) of the number of collected species (s) (Magurran, 206
176 tions and functions. Furthermore, such areas have piped drinking 2004). 207
177 water, but there are no sewer or garbage collection systems. Species richness was estimated by calculating of Margalef’s 208
index (DMg). This index was calculated through this equation: 209
(DMg) = (s − 1)/ln N (Magurran, 2004). 210
178 2.2. Sand fly collection
Beta diversity was also estimated by similarity between differ- 211
ent communities using Jaccard’s (Sj) and Sorensen’s Indices (Ss). 212
179 Sand flies were collected once a month using 90 sticky paper
Sj: a/(a + b + c) and Ss: 2a/(2a + b + c) are equations for the calcu- 213
180 traps from indoors (human dwelling and stables) and outdoors
lation of Jaccard’s and Sorensen’s Indices, respectively (Chao et al., 214
181 (rodent burrows or outside) during March 2012 to January 2013
2005). In these equations, ‘a’ is the number of species present in 215
182 from fixed places and once in October 2013 from random places
both communities; ‘b’ is the number present in community i and ‘c’ 216
183 in Shush and Khorramshahr Counties. Sixty traps were placed
is the number of species present in community j. 217
184 indoors (30 in human dwelling, 30 in stables) and 30 traps outdoors
Effects of human pressure on the biodiversity of sand 218
185 (rodent burrows in agricultural and natural habitats) or outsides in
flies species was calculated based on three habitats (urban, 219
186 urban and semi urban areas. The traps were set before sunset and
semi urban and natural) of Shush and Khorramshahr 220
187 collected in the next morning before the sunrise. The sand flies
Counties. 221
188 were removed using an entomological needle, washed in absolute
The urban area shows high degree of anthropization; it is an 222
189 acetone, and preserved in 70% ethanol. Samples were mounted
area with condensed human settlements in the town. The semi 223
190 using Puri’s medium (Smart et al., 1965) that was made at the
urban area represents a remote area from the town with almost 224
191 leishmaniasis unit of Department of Medical Entomology & Vec-
condensed localities and the Natural area is defined for the discrete 225
192 tor Control, School of Public Health, Tehran University of Medical
places from the town with reduced human settlements (Bueno Mari 226
193 Sciences. The sand flies were identified after 24 h using the keys
and Jimenez-Peydro, 2011). 227
194 of Theodor and Mesghali (1964) and Seyedi-Rashti and Nadim
Synanthropic index was calculated with the formula: 228
195 (1992).
SI = (2a + b − 2c)/2. In this equation ‘a’ is the percentage of collected 229
species in the urban area, ‘b’ is the percentage of collected species 230
in the semi urban area and ‘c’ is the percentage of collected species 231
196 2.3. Data process and analysis
in the natural area (Nuorteva, 1963). This index was calculated for 232
P. papatasi and P. alexandri. 233
197 For the collected sand flies from fixed places, alpha diversity
Synanthropic index varies between +100 to −100.This range 234
198 with three indices i.e. Shannon–Weiner (H), Margalef’s or richness
shows a strong preference for dense human settlements or higher 235
199 (DMg) and Evenness (E) were calculated using Microsoft office Excel
200 2007. degrees of domiciliation (+100) and complete avoidance of human Q3 236
environment or the lowest degree of domiciliation (−100) (Uribe-M 237
201 Shannon–Weiner index (H) uses this equation: H = −
et al., 2010; Bueno Mari and Jimenez-Peydro, 2011). 238
202 (pi × ln pi). ‘pi’ can be calculated by dividing ni, the number of
Please cite this article in press as: Jahanifard, E., et al., Diversity of sand flies (Diptera, Psychodidae) in southwest Iran with emphasis on
synanthropy of Phlebotomus papatasi and Phlebotomus alexandri. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.08.017
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239 3. Results Calculations of Jaccard’s and Sorensen’s coefficients showed 297
that the highest community similarity of sand flies (Isorenson = 0.95, 298
240 A total of 11213 sand flies were collected from fixed and ran- Ijaccard = 0.9) was observed between natural and agricultural ecosys- 299
241 dom places during March 2012 to January 2013. Eleven species tems of Shush County. The lowest similarity was also observed 300
242 were identified, of which 2 belonged to genus Phlebotomus and 9 to between urban area and natural ecosystem of Shush County (Sj = 0.3 301
243 genus Sergentomyia (Table 1). P. papatasi was the most predominant and Ss = 0.46). The comparison of similarity of sand flies population 302
244 species accounted for 40.76% of the identified sand flies, followed by between Shush and Khorramshahr indicated that maximum simi- 303
245 S. sintoni (36.26%), P. alexandri (9.96%), S. tiberiadis (7.47%), S. den- larity was observed between urban area of Shush and semi urban 304
246 tata (2.77%), S. iranica (2%), S. baghdadis (0.11%), S. clydei (0.53%), area of Khorramshahr (Sj = 0.75 and Ss = 0.86). Moreover, the low- 305
247 S. squamipleuris (0.07%), and S. christophersi (0.01%). Overall, the est similarity between the two counties was observed in the urban 306
248 number of males (6464) was more than females (4749). area of Khorramshahr and natural ecosystem of Shush (Sj = 0.3 and 307
Ss = 0.46) (Table 3). 308
249 3.1. Shush county
3.4. Synanthropic index 309
250 A total of 7678 sand flies were collected (23.63% indoors, 76.37%
251
outdoors). Eleven species (2 of G. Phlebotomus and 9 of G. Ser- In Shush County, synanthropic index of P. papatasi and P. 310
252
gentomyia) were found. P. papatasi (25.9%), P. alexandri (0.46%), S. alexandri were calculated to be −83.34 and −91.18, respectively. 311
253
sintoni (66.79%), S. squamipleuris (0.22%), S. iranica (0.34%), S. tiberi- Estimated synanthropic indices for these two collected species in 312
254
adis (1.89%), S. dentata (2.97%), S. christophersi (0.02%), S. theodori natural, semi urban and urban habitats of Khorramshahr County 313
255
(0.14%) and S. clydei (1.27%) were collected from rodent burrows were −69.84 and −85.89, respectively (Table 4). P. alexandri had the 314
256
and S. sintoni (66.79%) was the most frequent species. Eight species lower synanthropic index in comparison with P. papatasi in both 315
257
were found outdoors including: P. papatasi (4.23%), P. alexandri counties, suggesting the more adaptation of the species to urban 316
258 (0.11%), S. sintoni (12.6%), S. dentata (5.32%), S. squamipleuris (0.22%), environments. 317
259 S. tiberiadis (56.46%), S. iranica (20.3%) and S. clydei (0.76%). Sergen-
260 tomyia tibriadis was the predominant species found outdoors and
4. Discussion 318
261 S. christophersi was a new record for this county. In peridomestic
262 areas of the county (stables), the most common species was P. pap-
Controlling vectors with exophilic behavior such as sand flies is 319
263 atasi (83.64%), followed by S. tiberiadis (10.62%), S. sintoni (3.66%), P.
very difficult. Exophilic and exophagic behaviors of sand flies led 320
264 alexandri (1.15%), S. iranica (0.62%), S. squamipleuris (0.15%), S. den-
them to avoid any controlling attempts such as chemical controls. 321
265 tata (0.08%), and S. baghdadis (0.08%). Moreover, P. papatasi (57.14%)
To reduce their human health impact, avoidance of contact between 322
266 and S. sintoni (17.03%) were found to be dominant species in human
human and vectors seems to be the best way. In addition to sand 323
267 dwellings (Fig. 2).
flies diversity, one of the main measures of biology and behavior of 324
sand flies is their synanthropy. Understanding the ability of changes 325
268 3.2. Khorramshahr county
in synanthropy behavior of sand flies helps us to control the vec- 326
tor. In this regard, we carried out the first study on diversity and 327
269 An overall 3535 sand flies were collected (69.76% indoors,
synanthropy index of sand flies in southwest Iran. 328
270 30.24% outdoors). Seven species of sand flies (2 of G. Phleboto-
Javadian and Nadim (1975) reported 16 phlebotomine species 329
271 mus and 5 of G. Sergentomyia) were identified. The seven species
(6 G. Phlebotomus and 10 G. Sergentomyia) in the area while in the 330
272 found outdoors (rodent burrows) included: P. papatasi (35.2%), P.
present study,11 species including (2 of G. Phlebotomus and 9 of G. 331
273 alexandri (17.34%), S. sintoni (35.72%), S. dentata (9.97%), S. baghdadis
Sergentomyia were collected and identified. Based on our data, the 332
274 (0.52%), S. tiberiadis (1.04%), and S. iranica (0.21%). The most preva-
biodiversity of phlebotominae sand flies was found to be higher in 333
275 lent species were P. papatasi (51.89%) and S. sintoni (33.02%). The
Shush than Khorramshahr. Javadian et al. (1974) reported 7 species 334
276 following 6 species were collected indoors: P. papatasi, P. alexan-
including P. sergenti, P. tobbi, P. neglectus, P. salehi. Sergentomyia 335
277 dri, S. sintoni, S. tiberiadis, S. baghdadis, S. dentata. The predominant
antenata, S. palestinensis and S. mervynae in these 2 counties but 336
278 species indoors (stables) were P. papatasi (59.5%) and P. alexandri
there were changes after 42 years, and S. clydei and S. christophersi 337
279 (36.03%). P. papatasi, P. alexandri, S. sintoni, S. baghdadis, S. tiberiadis
were new records in the present study. The change on the composi- 338
280 and S. dentata were found in human dwellings, among which P. pap-
tion of sand flies maybe due to human intervention in their natural 339
281 atasi (64.11%) and P. alexandri (26.32%) were predominant species habitat. 340
282 (Fig. 3).
Our data indicated that after more than 4 decades P. papatasi 341
and P. alexandri are still active in both counties, with P. papatasi 342
283 3.3. Biodiversity of the sand flies communities to be dominant species both outdoors and indoors. The average 343
humidity in Khorramshahr and Shush Counties was calculated to be 344
◦ ◦
284 Only three species of sand flies were collected from the urban 44% and 46.45% but the mean temperature was 27.5 C and 26.1 C, 345
285 area of Shush; however, according to analysis of Shannon–Weiner respectively, suggesting the species preference of high temperature 346
286 index (H), species diversity in this area was higher compared to and average humidity, which can be found in semi-arid and arid 347
287 other habitats (H = 2.561, E = 2.331, DMg = 0.358). Due to highest areas. Our results were in consistence with the previous finding 348
288 species richness in other habitats (DMg = 1.03–1.08), it seems that by Singh (1999) in India. In the present study, P. alexandri and P. 349
289 it is better to compare the indices among natural, agricultural and papatasi were found from −17 to 407 m above sea level; however, P. 350
290 semi urban habitats. Considering the highest evenness and richness alexandri recorded between 3 and 1394 m and P. papatasi between 351
291 (H = 1.452, E = 0.698, DMg = 1.03) in semi urban area of Shush, it is 8 and 1756 m above the sea level in other parts of Iran (Yaghoobi- 352
292 not surprising that this habitat is of the maximum species biodiver- Ershadi et al., 2005; Kassiri and Javadian, 2012; Yaghoobi-Ershadi, 353
293 sity. The analysis of ␣ biodiversity showed that agricultural area of 2012; Kavarizadeh et al., 2013). 354
294 Khorramshahr County had the highest diversity due to maximal The distribution of P. papatasi highly depends on environ- 355
295 richness and diversity and also relatively high evenness (H = 1.209, ment factors particularly relative humidity and temperature (Cross 356
296 E = 0.621, DMg = 0.794) (Table 2). et al., 1996). Akhoundi et al. (2012) has described the influence of 357
Please cite this article in press as: Jahanifard, E., et al., Diversity of sand flies (Diptera, Psychodidae) in southwest Iran with emphasis on
synanthropy of Phlebotomus papatasi and Phlebotomus alexandri. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.08.017
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Fig. 2. Fauna and percent of collected sand flies from (i) indoor (stables), (ii) indoor (human dwellings), (iii) outdoor (rodent burrows), (iv) outdoor in fixed and random
places of Shush County, Khuzestan Province, Iran, March 2012 to January 2013.
Fig. 3. Fauna and percent of collected sand flies from (i) indoor (stables), (ii) indoor (human dwellings), (iii) outdoor (rodent burrows), (iv) outdoor in fixed and random
places of Khorramshahr County, Khuzestan Province, Iran, March 2012 to January 2013.
Please cite this article in press as: Jahanifard, E., et al., Diversity of sand flies (Diptera, Psychodidae) in southwest Iran with emphasis on
synanthropy of Phlebotomus papatasi and Phlebotomus alexandri. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.08.017
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Table 1
Species composition and relative abundance of phlebotomine sand flies in the study areas of Khuzestan Province, March 2012 to January 2013.
Species Male Female Total %
No % No %
P. papatasi 3553 31.68 1019 9.08 4572 40.76
P. alexandri 825 7.36 291 2.6 1116 9.96
S. sintoni 1317 11.75 2748 24.51 4065 36.26
S. tiberiadis 555 4.95 283 2.52 838 7.47
S. dentata 51 0.45 260 2.32 311 2.77
S. baghdadis 0 0 12 0.11 12 0.11
S. iranica 133 1.19 91 0.81 224 2
S. squamipleuris 1 0.01 7 0.06 8 0.07
S. clydei 22 0.2 37 0.33 59 0.53
S. theodori 6 0.05 1 0.01 7 0.06
S. christophersi 1 0.01 0 0 1 0.01
Total 6464 57.65 4749 42.35 11213 100
Table 2
The results of alpha biodiversity for sand flies species in four habitats of Shush and Khorramshahr Counties, Khuzestan Province, Iran, March 2012 to January 2013.
County Habitat Shannon–Weiner biodiversity index (H) Evenness (E) Richness (DMg)
Shush Natural 0.867 0.376 1.08
Agricultural 1.246 0.599 1.04
Semi urban 1.452 0.698 1.03
Urban 2.561 2.331 0.358
Khorramshahr Natural 0.944 0.527 0.696
Agricultural 1.209 0.621 0.794
Semi urban 0.978 0.706 0.582
Urban 0.812 0.739 0.522
Table 3
The results of beta diversity for sand flies species in four habitats of Shush and Khorramshahr Counties, Khuzestan Province, Iran, March 2012 to January 2013.
County/Habitat Shush Khorramshahr
Natural Agricultural Semi urban Urban Natural Agricultural Semi urban Urban
Shush Natural – 0.9 0.8 0.3 0.45 0.54 0.4 0.3
Agricultural 0.95 – 0.88 0.33 0.5 0.6 0.44 0.33
Semi urban 0.88 0.94 – 0.38 0.55 0.33 0.5 0.38
Urban 0.46 0.5 0.55 – 0.5 0.43 0.75 0.5
Khorramshahr Natural 0.63 0.66 0.71 0.66 – 0.86 0.66 0.5
Agricultural 0.71 0.75 0.8 0.6 0.92 – 0.57 0.43
Semi urban 0.67 0.62 0.66 0.86 0.8 0.72 – 0.75
Urban 0.46 0.5 0.55 0.66 0.66 0.6 0.86 –
–Data above the diagonal represents the Jaccard index and data below the diagonal represents the Sorensen index.
Table 4
Synanthropic index of two Phlebotomus species in natural ecosystem, semi urban and urban habitats of Khuzestan Province, Iran, March 2012 to January 2013.
Species Shush county Khorramshahr county
Natural ecosystem Semi urban area Urban area Total SI Natural ecosystemSemi urban area Urban area Total SI
N % N % N % N % N % N %
P. papatasi 1417 89.23 155 9.76 16 1.01 1588 −83.34 777 84.92 106 11.58 32 3.5 915 −69.84
P. alexandri 48 94.12 3 5.88 0 0 51 −91.18 403 90.97 35 7.9 5 1.13 443 −85.89
358 altitude on spatial distribution of phlebotomines in northwest Iran. for instance, abundance and distribution of vertebrate hosts (Cross 372
359 There was inverse correlation between temperature and altitude et al., 1996; Ghosh et al., 1999). It seems that environmental cir- 373
− ◦
360 ( 6 C per 100 m). Mean humidity and temperature in Shush and cumstances such as groundwater and surface water, land cover, 374
361 Khorramshahr were more or less the same during the study, but land use and also abiotic factors like humidity and organic matter 375
362 annual precipitation in Shush (236.8 mm) was more than two folds of soil can affect the distribution of sand flies in Shush County. It 376
363 that in Khorramshahr (112.4 mm). Kassem et al. (2012) have shown should be mentioned that during the last five years the recorded 377
364 that elevation and climatic conditions were limiting determinants numbers of ZCL cases in Shush County (955 cases) has been more 378
365 for the distributions of sand flies in southern Sinai. They indicated than two folds that in Khorramshahr (445 cases) (Health Centers of 379
366 the highly diverse landscape and environmental factors (geology, Shush & Khorramshahr, unpublished data). 380
367 hydrology, elevation, maximum and minimum air temperature, Toprak and Ozer (2007) revealed that P. alexandri was present 381
368 relative humidity and annual precipitation) have been associated in more urban areas of Sanliurfa Province of Turkey rather than 382
369 with species diversity of sand flies in some parts of Egypt. High rural areas, whereas in our investigation this species was observed 383
370 frequency of sand flies can be correlated with such physical fac- with limited number in urban areas of Khorramshahr and was not 384
371 tors as availability of resting and breeding places; biotic factors, found in urban areas of Shush. This may be due to destruction of 385
Please cite this article in press as: Jahanifard, E., et al., Diversity of sand flies (Diptera, Psychodidae) in southwest Iran with emphasis on
synanthropy of Phlebotomus papatasi and Phlebotomus alexandri. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.08.017
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386 the natural habitats of this species in urban areas because of the Epidemiological features together with similarity indices in 452
387 extent the county. various areas of the county lead us to conduct uniform control 453
388 The urban area of Shush County is of highest biodiversity, even- programs to more similar areas. 454
389 ness and the lowest species richness. It shows that the lowest
390
species number in this area became more adapted with environ- Acknowledgements 455
391 mental conditions. The highest species richness was in semi urban
392 area of this county which shows the high species number in periph-
The authors are grateful to Dr. A. Kamali responsible person 456
393 eral area of the county. It can be concluded that natural habitat is
for zoonoses in Khuzestan Province and staff of health centers in 457
394 in stress of continuously drought in Shush County. This condition
the counties of Shush and Khorramshahr: A. Hejazi, H. Mostahfez, 458
395 may affect the source feeding of sand flies such as rodents that may
M. Maleki, A. Vadian and Sh. Kazemi, for their assistance during 459
396 move to well irrigated neighboring areas and agricultural fields. It
sampling of sand flies in the field. This study was funded and sup- 460
397 seems that the reduction of species biodiversity and evenness of
ported by Tehran University of Medical Sciences (TUMS): Grant no: Q4 461
398 sand flies in natural area of Shush County is due to such factors as 90-04-27-16311. 462
399 mentioned above.
400 The species biodiversity and species richness of sand fly com-
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Please cite this article in press as: Jahanifard, E., et al., Diversity of sand flies (Diptera, Psychodidae) in southwest Iran with emphasis on
synanthropy of Phlebotomus papatasi and Phlebotomus alexandri. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.08.017