Checklist and Geographical Distribution of Phlebot
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Tehran University of Medical Sciences
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Abstract
Phebotomine sand flies are reported as the vectors of different kinds of leishmaniasis and
arboviruses to human. Three forms of leishmaniasis, namely: visceral, zoonotic cutaneous and
anthroponotic cutaneous affect Esfahan province. Antibodies against three arbovirouses, Nepales,
Sicilian and Karimabad, were found from serum and blood specimen residents in this province too.The
aim of this study was to prepare a checklist and geographical distribution of Phlebotomine sand flies as
vectors of the agents from Esfahan province. In the field work, sand flies were collected by sticky
paper traps from 10 collection stations of Natanz, Mobarakeh, Shahreza and Esfahan city areas of
Esfahan province during 2006 to 2013. Also literature review was done on all publish reports which
have been done by researchers on Phlebotomine sand flies in this province during 1968 to 2013. A total
of 170380 specimen sand flies revealed 28 species are in this province. Phlebotomus papatasi as the
main vector of zoonotic cutaneous leishmaniasis and arbovirouses and also P. sergenti as the main
vector of anthroponotic cutaneouse leishmaniasis were collected from all areas of this province. Also
P. alexandri, P. major, P. kandelaki and P. keshishiani as suspected vectors of visceral leishmaniasis
in Iran were found in this province.The geographical distribution of each 28 species of sand flies in
Esfahan province and some important notes of them is demonstrated in this article.
Key Words: Checklist, Geographical Distribution, Phlebotomine Sand flies, Esfahan Province, Iran
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Introduction
Sand flies are classified in oder Diptera, suborder Nematocera, family Psychodidae and subfamily
Phlebotominae (Seyedi-Rashti Nadim, 1992). The subfamily contains 5 genera which Phlebotomus
Rondani & Berte, 1840 (with 10 subgenus), and Sergentomyia France & Parrot, 1920 (with 7 subgenus
& 1 species-group) are in the old world (Lewis et al., 1977; Lewis, 1982).
The Phlebotomine sand flies are blood-sucking insects (Artemiev, 1978). The identification of sand
fly species is epidemiologically very important because less than 10 percent of over 800 species
described are responsible for the transmission of human pathogens such as flagellate protozoa of the
genus Leishmania (Kato et al., 2010) in more than 80 countries in the old and new world (Depaquit
et al., 2010).
Three species of leishmania have been incriminated as the causative agents of human leishmaniasis
infection (Nadim & Seyedi-Rashti, 1971) namely: Visceral (VL due to L. infantum), Zoonotic
Cutaneous (ZCL due to L. major) and Anthroponotic Cutaneous (ACL due to L. tropica) (W.H.O,
2004) in Iran.
In Esfahan province the VL cases were not indigenous and it had sporadic cases that most came in
the summer time from neighboring provinces (Tabatabaii et al., 1975) but recently some
autochthonous cases were reported from Shahreza in this province (Emami & Yazdi, 2008).
A rural area to the north and east of the city of Esfahan, among the foothills of the Karkas
mountains in central Iran is hyper endemic area of Zoonotic Cutaneous leishmaniasis (ZCL) because in
this area intensities transmission occurs, so that many indigenous residents acquire the disease before
the age of five and almost 80% of all reported cases of ZCL in this country is from Esfahan province
(Nadim et al., 1988; Yaghoobi-Ershadi et al., 2005).
Anthroponotic Cutaneouse leishmaniasis (ACL) reported from Esfahan city on the basis of
epidemiological data, clinical manifestation (Zahraei-Ramazani et al. 2007) confirmed by isoenzyme
(Hatam et al., 2005), and also L. tropica parasite isolated from active lesions of infected patients in the
city of Esfahan (Farid-Moaeir et al., 1997).
Sand flies also are vectors of some viruses and the frequency of human infection with Phlebotomus
fever viruses is high in Iran (Tesh et al., 1976).
In Esfahan, antibodies against three, Nepales, Sicilian, and Karimabad, Phlebotomus fever virus
serotypes were found from serum and blood specimen residents (Tesh et al., 1976). The highest
Karimabad infections rate were found in Esfahan province suggesting that the virus is endemic in this
region (Tesh et al., 1976) in Esfahan province.
Sand flies were first recorded by Adler, Theodor and Lourie in 1930 from Iran and until now there
are 56 reported species of sand flies belonging to the genus Phlebotomous (subgenera Adlerius,
Euphlebotomus, Larrousius, Paraphlebotomus, Phlebotomus, Synphlebotomus) and genus
Sergentomyia (subgenera Grassomyia, Parrotomyia, Parvidens, Rondanomyia, Sergentomyia,
Sintonius) (Kassiri et al., 2011a; Zahraei-Ramazani et al., 2015).
Initially, the fauna and distribution of Phlebotominae sand flies have been recorded from different
areas of Esfahan province since 1968. Until now different studies have been done on the sand flies in
this province by researchers. So, in this paper we are going to prepare a checklist of Phlebotominae
sand flies species and demonstrate their geographical distribution and some important notes of them by
not only field work but also literature review of all articles that have been published from different
areas of this province.
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Zahraei-Ramazani et al: Checklist and Geographical Distribution of Phlebotomine Sand flies (Diptera: Psychodidae)…
mountains and plains, with an average elevation of 1600 m. It is in an area of approximately 107029
square kilometers (SCI, 1965c; Ostandari Esfahan, 2012; IRIMO, 2012). The province is bounded by
Markazi, Qom, and Semnan provinces in North, Lorestan province in West, Kohkiluyeh and Boyer-
Ahmad and Fars provinces in South, Yazd in East, and Chahar mahalobakhtiari and Khuzestan in
Southwest. The center of the province is Esfahan city (Figure 1).
Esfahan province can be divided into three topographic and climatic regions based on their distance
from the Zagros mountains in the west and the great desert in the East; (1) semi-humid and cold areas
encompassing western and southern valleys; (2) the arid areas along the edge of the central desert; (3)
the semi-arid region of the oasis of Esfahan marked by a moderate climate and four distinct seasons.
Relative humidity varies between 25 and 62 percent (Ministry of Agricultural Jahad, 2012) (Table 1,
Figure 1).
Mounting:
The head and genitalia of individual sand flies were cut off within a drop of ethanol on a clean slide
then they transferred to a drop of puri’s media between a slide and cover slip (Smart et al. 1965).
Identification of specimens was done with the available taxonomic keys (Theodor & Mesghali, 1964;
Artemiev, 1978; Lewis, 1982; Seyedi-Rashti & Nadim, 1992).
Literature review:
Also simultaneously the literature review was done on all published reports which have been done
by the researchers on Phlebotomine sand flies in Esfahan province during 1968 to 2013.
Results
In the last field research, a total of 716 adults sand fly were collected. 53.4% of the specimens were
belonging to Phlebotomus genus species while 46.6% were belonging to Sergentomyia genus species
(Zahraei Ramazani et al., 2015).
The result of our literature review on the Phlebotominae sand flies vectors in Esfahan province
shows that Nadim et al. (1968) were the first researchers who studied on fauna of sand flies in the
different area of this province (Esfahan, Fereidan, Ardestan, Naein, Shahreza, Najafabad). Baghaei et
al. (1996) worked and published in Persian on the fauna of Rodashtein area (along the Zayandeh Road
River from Esfahan city to the Ghave Khoni Swampland). Yaghoobi & javadian et al. (1997) worked
on the fauna of Borkhar area, Yaghoobi et al. (1998) studied on fauna of Ardestan area, Eshghi (1998)
did his MSc thesis on fauna of Shahreza area (Full text in Persian), Yaghoobi & Akhavan et al. (1999)
studied on the fauna of Natanz area, Yaghoobi et al. (2001) found the fauna of Jarghoyeh (Full text in
Persian), Zahraei Ramazani et al. (2006) worked on the fauna of Esfahan city, Abdoli et al. (2007)
studied on the fauna of Kuhpayeh area, Emami and Yazdi (2008) worked on the fauna of Shahreza, and
Emami et al (2009) found the fauna of Mobarakeh. In the latest research on vectors of leishmaniasis
leading to identify the P.(Adlerius) kabulensis species as a new record for city of Natanz and Iran
country (Zahraei Ramazani et al., 2015).
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Journal of Entomological Research Volume 7, Issue 4, 2016, (69-82)
As a result of prepare a checklist of the Phlebotomine sand flies in Esfahan province, taxonomic
position, geographical distribution (Figure 1), and some notes on importance of each species are given
in the present paper.
So during this field study and the result of the review articles, 170380 adult sand flies were
identified and a total of 28 species of sand flies representing 9 subgenus (5 subgenus of Phlebotomus
genus and 4 subgenus of Sergentomyia genus) have been recorded in collections made in 12 areas in
this province. These species are listed below in alphabetical order of genera and then species, and
information on their geographic distribution, climatic and temperature variation is summarized in the 3
tables and illustrated in one Figure.
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Journal of Entomological Research Volume 7, Issue 4, 2016, (69-82)
Table 1- The geographic, climatic and temperature variation in different areas of Phlebotominae sand flies fauna in Esfahan Province
Esfahan city
Area
Mobarakeh
Najafabad
Jarghoyeh
Kuhpayeh
Shahreza
Ardestan
Fereidan
Borkhar
Kashan
Natanz
Naein
Data
Latitude(N) 32º 37' 33º 59' 33º 32' 32º 58' 32º 38' 31º 59' 32º 21’ 32º 24’ 32º 43' 32º 40' 33º 22' 32º 51'
Longitude(E) 51º 40' 51º 27' 51º 54' 50º 25' 51º 22' 51º 50' 51º 30' 52º 37' 52º 26' 51º 52' 52º 24' 53º 05'
Elevation 1550.4 982.3 1684.9 2390 1650 1845.2 1670 1250 1750 1543 1381 1549
Monthly Total of
Precipitation (mm)
122.8 138.4 195.3 350 153.5 144 150 760 110 107.6 112.3 98.7
Average of Minimum
Temperature( Cº)
9.1 12.1 10.7 4.4 6.2 7 11 6.9 6.7 6 10 9.8
Average of Maximum
Temperature( Cº)
23.4 26.1 20.2 17.3 12.8 22.3 26.3 24.2 23.9 23.9 25 23.4
Table 2- Distribution of various species of Genus Phlebotomus sand flies in different areas of the province of Esfahan
Esfahan city
Kashan
Natanz
Fereidan
Najafabad
Shahreza
Mobarakeh
Jarghoyeh
Kuhpayeh
Borkhar
Ardestan
Naein
Area
Sand fly
Species
P.papatasi + + + + + + + + + + + +
P.sergenti + + + + + + + + + + + +
P.caucasicus + - + - + + - + + + + +
P.mongolensis - - - - + + + + + + - -
P.kandelakii + + + + - + - - + + - -
P.anderjevi - - - - - + - - - - - -
P.ansarii - + + + + + - + + + + -
P.major - + + - - + - - + + + +
P.alexandri + + + - + + + - + + + +
P.kazeruni - - - - - + - - - + - -
P.jacuseli - + - - + - - - - - - -
P.halepensis - + + + - + - - - - - -
P.brevis - + - - - - - - - - - -
P.tobbi - + - - - - - - - - - -
P.longiductus - + - - - - - - - - - -
P.salehi - - - - - - + - - - - -
P.keshishiani - - - - - + - - - - - -
P.kabulensis - - + - - - - - - - - -
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Table 3- Distribution of various species of Genus Sergentomyia sand flies in different areas of the province of Esfahan
Esfahan city
Mobarakeh
Najafabad
Jarghoyeh
Kuhpayeh
Shahreza
Ardestan
Fereidan
Borkhar
Kashan
Natanz
Area
Naein
Sand fly
Species
S. sintoni + + + - + + + + + + + +
S. dentata + + + + - + + - + + - +
S. povlovskyi + + + + - + + - + + + -
S. clydei + + - - - - - - - - - -
S. sumbarica - - - - - - - - - - + -
S. palestiansis - + + - - + - - - - + -
S. baghdadis + - - - - + - - - - - -
S. grekovi - - + - - - - - - - - -
S. tiberiadis - + + - - - - - - - - -
S. christophersi - - - - - - + - - - - -
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Fig. 1- Geographical distribution and areas of Phebotominae sand fly collection in Esfahan province
Conclusion
The geographical distribution of each 28 species of sand flies in Esfahan province and some
important notes of them is demonstrated in this article.
Phlebotomus papatasi as the main vector of zoonotic cutaneous leishmaniasis and arbovirouses and
also P. sergenti as the main vector of anthroponotic cutaneouse leishmaniasis were collected from all
areas of this province. Also P. alexandri, P. major, P. kandelaki and P. keshishiani as suspected
vectors of visceral leishmaniasis in Iran were found in this province.
Acknowledgment
The authors would like to appreciate director and stuff of Esfahan Health Research station, National
Institute of Health Research. Thanks are also to D. Leshan Wannigama, PhD student in Medical
Science in Chulalongkorn University for completing the sand flies geographical distribution map. This
work was supported by Tehran University of Medical Sciences. The authors declare that there is no
conflict of interests.
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-2داﻧﺸﻴﺎر ،ﮔﺮوه ﺣﺸﺮهﺷﻨﺎﺳﻲ ﭘﺰﺷﻜﻲ و ﻣﺒﺎرزه ﺑﺎ ﻧﺎﻗﻠﻴﻦ ،داﻧﺸﻜﺪه ﺑﻬﺪاﺷﺖ و اﻧﺴﺘﻴﺘﻮ ﺗﺤﻘﻴﻘﺎت ﺑﻬﺪاﺷﺘﻲ ،داﻧﺸﮕﺎه ﻋﻠﻮم ﭘﺰﺷﻜﻲ ﺗﻬﺮان
ﭼﻜﻴﺪه
ﭘﺸﻪ ﺧﺎﻛﻲﻫﺎي ﻓﻠﺒﻮﺗﻮﻣﻴﻨﻪ ﻧﺎﻗﻠﻴﻦ اﻧﻮاع ﻟﻴﺸﻤﺎﻧﻴﻮزﻫﺎ و آرﺑﻮوﻳﺮوسﻫﺎ ﺑﻪ اﻧﺴﺎن ﻣﻲﺑﺎﺷﻨﺪ .ﺳﻪ ﻧﻮع ﻟﻴﺸﻤﺎﻧﻴﻮز ﺟﻠﺪي روﺳﺘﺎﻳﻲ،
ﺟﻠﺪي ﺷﻬﺮي و ﻧﻴﺰ اﺣﺸﺎﻳﻲ در اﺳﺘﺎن اﺻﻔﻬﺎن وﺟﻮد دارد .ﻫﻤﭽﻨﻴﻦ آﻧﺘﻲ ﺑﺎديﻫﺎي ﺿﺪ ﺳﻪ ﻧﻮع آرﺑﻮوﻳﺮوس ﻧﭙﺎل ،ﺳﻴﺴﻴﻞ و
ﻛﺮﻳﻢ آﺑﺎد در ﺧﻮن و ﺳﺮم ﺳﺎﻛﻨﻴﻦ اﻳﻦ اﺳﺘﺎن ﻳﺎﻓﺖ ﻣﻲﺷﻮد .ﻫﺪف از اﻳﻦ ﻣﻄﺎﻟﻌﻪ ﺗﻬﻴﻪ ﻓﻬﺮﺳﺘﻲ ﻛﺎﻣﻞ از ﭘﺸﻪ ﺧﺎﻛﻲﻫﺎي ﻓﻠﺒﻮﺗﻮﻣﻴﻨﻪ
و ﻧﻴﺰ ﺗﻮزﻳﻊ ﺟﻐﺮاﻓﻴﺎﻳﻲ آنﻫﺎ در اﺳﺘﺎن اﺻﻔﻬﺎن ﻣﻲﺑﺎﺷﺪ .در ﻣﻄﺎﻟﻌﻪ ﺻﺤﺮاﻳﻲ ،ﭘﺸﻪ ﺧﺎﻛﻲﻫﺎ ﺗﻮﺳﻂ ﺗﻠﻪ ﭼﺴﺒﺎن از 10ﻣﻜﺎن
ﻣﺨﺘﻠﻒ در ﻧﻄﻨﺰ ،ﻣﺒﺎرﻛﻪ ،ﺷﻬﺮﺿﺎ و ﻧﻴﺰ ﺷﻬﺮ اﺻﻔﻬﺎن ،اﺳﺘﺎن اﺻﻔﻬﺎن ﻃﻲ ﺳﺎلﻫﺎي 1385ﺗﺎ 1392ﺟﻤﻊآوري ﮔﺮدﻳﺪﻧﺪ .ﺑﻪﻋﻼوه
ﺑﺎ ﻣﻄﺎﻟﻌﻪ ﻛﺘﺎﺑﺨﺎﻧﻪاي و ﻣﺮاﺟﻌﻪ ﺑﻪ ﻛﻠﻴﻪ ﻣﻘﺎﻻت و ﻧﻮﺷﺘﻪﻫﺎي ﻣﺤﻘﻘﻴﻦ ﻣﺨﺘﻠﻒ ﻓﻬﺮﺳﺘﻲ از ﮔﻮﻧﻪﻫﺎي ﭘﺸﻪ ﺧﺎﻛﻲ ﮔﺰارش ﺷﺪه ﻃﻲ
ﺳﺎلﻫﺎي 1347ﺗﺎ 1392ﺷﻨﺎﺳﺎﻳﻲ و ﻳﺎدداﺷﺖ ﮔﺮدﻳﺪ .در ﻛﻞ از ﺗﻌﺪاد 170380ﻧﻤﻮﻧﻪ ﭘﺸﻪ ﺧﺎﻛﻲ ﺻﻴﺪ ﺷﺪه از اﻳﻦ اﺳﺘﺎن ،ﺗﻌﺪاد
28ﮔﻮﻧﻪ ﮔﺰارش ﺷﺪه اﺳﺖ .ﭘﺸﻪ ﺧﺎﻛﻲ Phlebotomus papatasiﻧﺎﻗﻞ ﻗﻄﻌﻲ ﻟﻴﺸﻤﺎﻧﻴﻮز ﺟﻠﺪي روﺳﺘﺎﻳﻲ و آرﺑﻮوﻳﺮوﺳﻬﺎ
ﺑﻪﻋﻼوه ﭘﺸﻪ ﺧﺎﻛﻲ Phlebotomus sergentiﻧﺎﻗﻞ ﻟﻴﺸﻤﺎﻧﻴﻮز ﺟﻠﺪي ﺷﻬﺮي از ﺗﻤﺎم ﻣﻨﺎﻃﻖ اﺳﺘﺎن اﺻﻔﻬﺎن ﺻﻴﺪ ﮔﺮدﻳﺪه اﺳﺖ.
ﻫﻤﭽﻨﻴﻦ ﭘﺸﻪ ﺧﺎﻛﻲﻫﺎي ) P. major ،P. kandelakiاﺣﺘﻤﺎﻻ P. keshishiani ،(P. neglectusو ﻧﻴﺰ P. alexandriﻧﺎﻗﻠﻴﻦ
ﻟﻴﺸﻤﺎﻧﻴﻮز اﺣﺸﺎﻳﻲ در اﻳﺮان ﻧﻴﺰ از اﺳﺘﺎن اﺻﻔﻬﺎن ﺻﻴﺪ ﺷﺪهاﻧﺪ .اﻧﺘﺸﺎر ﺟﻐﺮاﻓﻴﺎﻳﻲ اﻳﻦ 28ﮔﻮﻧﻪ ﭘﺸﻪ ﺧﺎﻛﻲ و ﻧﻴﺰ ﺑﺮﺧﻲ از
ﻳﺎدداﺷﺖﻫﺎي ﻣﻬﻢ از آنﻫﺎ در اﻳﻦ ﻣﻘﺎﻟﻪ آورده ﺷﺪه اﺳﺖ.
واژهﻫﺎي ﻛﻠﻴﺪي :ﭼﻚ ﻟﻴﺴﺖ ،اﻧﺘﺸﺎر ،ﭘﺸﻪ ﺧﺎﻛﻲﻫﺎي ﻓﻠﺒﻮﺗﻮﻣﻴﻨﻪ ،اﺳﺘﺎن اﺻﻔﻬﺎن
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