Acta Tropica 132 (2014) 131–139

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Spatial and temporal distributions of phlebotomine sand flies (Diptera: Psychodidae), vectors of leishmaniasis, in Iran Ameneh Karimi, Ahmad Ali Hanafi-Bojd ∗ , Mohammad Reza Yaghoobi-Ershadi, Amir Ahmad Akhavan, Zahra Ghezelbash Department of Medical Entomology & Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

a r t i c l e

i n f o

Article history: Received 18 August 2013 Received in revised form 4 January 2014 Accepted 14 January 2014 Available online 24 January 2014 Keywords: Sand fly vectors Leishmaniasis Database Iran

a b s t r a c t Leishmaniasis is a major vector-borne disease and health problem in Iran. Studies on sand flies, as the vectors of the disease, began in the Northern and Western parts of the country in 1930 and have been continued up to now. Concerning many published information in the field of sand flies, providing a digital database for the country will help the public health authorities to make more correct and prompt decisions for planning leishmaniasis control programs as well as modeling and forecasting of transmission potential across the country. All published data on phlebotomine sand flies of Iran were collected. A database was then designed in Excel format, including all available information regarding sand flies. The valid data were transferred to ArcGIS9.3 to prepare the first spatial database of sand flies of Iran. The IrSandflybase includes 131 papers, 2 abstracts and 71 PhD/MSc theses, reporting studies conducted during 1930–2012. This database contains different available data covering all aspects of ecology and biology of 50 sand fly species in two genera of Phlebotomus and Sergentomyia in the country. The temporal activity of sand flies is reported 9 months in warm regions of the southern part, while it may reduce to 7–8 months in central plateau or 4–5 months in cold areas of the northwest. Occasional studies reported rare species from the borderlines of Iran. It seems that changing the climate due to global warming may affect the spatial distribution of different species and expand it into the country, the issue that can be followed by an updated database. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Of approximately 800 sand fly species in the world, about 50 have been concerned as vectors of leishmaniasis (Myler and Fasel, 2007). A sand fly species can be classified as specific or permissive vector of leishmaniasis according to parasite–sand fly interactions (Volf and Peckova, 2007). Iran is facing both form of leishmaniasis: cutaneous and visceral. The incidence of cutaneous leishmaniasis (CL) was varied from 0.002 to 1.337 during 2001–2011, while these values was found to be 0–0.03486 for visceral leishmaniasis (VL) in different provinces of Iran (Ministry of Health, unpublished data). Study of sand flies in Iran began in the North and West of the country in 1930 and have been continued up to now. The results of the studies showed that two genera Phlebotomus and Sergentomyia are

∗ Corresponding author at: Department of Medical Entomology & Vector Control, School of Public Health, Tehran University of Medical Sciences, P.O. Box 6446-14155, Tehran, Iran. Tel.: +98 21 42933167; fax: +98 21 88951393. E-mail address: aahanafi[email protected] (A.A. Hanafi-Bojd). 0001-706X/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.actatropica.2014.01.004

present in the country, comprising 44 confirmed species (YaghoobiErshadi, 2012). Some species of Phlebotomus play their role in the transmission cycle of leishmaniasis to humans as well as establishing the zoonotic cycle (rodents, canines) of the disease (Rassi and Hanafi-Bojd, 2006; Yaghoobi-Ershadi, 2012). Although there are reports of parasitic infection in Sergentomyia species (Mesghali et al., 1967; Nadim et al., 1968; Seyedi-Rashti et al., 1971; Rassi et al., 1997; Maleki Ravasan et al., 2008), these sand flies are introduced as vectors of lizard leishmaniasis. In addition to leishmaniasis, sand flies are introduced as vectors of sand fly fever in Iran as well (Javadian et al., 1977; Tesh et al., 1977a, 1977b). Despite many published information in the field of sand flies in the country, and different spatial distribution of vector species, providing a digital database will help the public health authorities to make more correct and prompt decisions for planning the disease control programs. Also modeling and forecasting of transmission potential as well as potential distribution of different species, especially exotic vectors, will be applied using the database. Overlaying the spatial distribution of a given vector, with the updated environmental and climatic layers that are involved in the disease transmission, will provide an up-to-date source for

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3. Results

Fig. 1. Location of Iran in Asia (http://commons.wikimedia.org).

prediction and modeling transmission potential. Therefore we began to establish the first database for Phlebotominae sand flies (Diptera: Psychodidae) of Iran, vectors of leishmaniasis, as an important neglected disease in the country. 2. Materials and methods Iran is the 18th largest country in the world in terms of area at 1,648,195 km2 (636,372 m2 ), located in Asia between latitudes of 25◦ 3 and 39◦ 47 North, and 44◦ 5 and 63◦ 18 east. The country has a population of more than 77 million, is bordered on the north by Armenia, Azerbaijan and Turkmenistan; on the east by Afghanistan and Pakistan, on the south by the Persian Gulf and the Gulf of Oman, on the west by Iraq and on the northwest by Turkey (Fig 1). The data collection was made to gather all published documents, papers, thesis and abstracts on phlebotomine sand flies of Iran till 2012. Search engines including Google scholar, Pubmed, Elsevier, IranMedex, SID and Scopus were used. Also detailed information about MSc/PhD thesis was collected from the libraries of School of Public Health, Tehran University of Medical Sciences (TUMS), as well as Tarbiat Modarres University, where it is supported in the field of medical entomology by TUMS. To avoid false data, one of the main inclusion criteria was to enter information which published by experts in the field of sand fly taxonomy. A database was designed in Excel format, including all available data regarding sand flies fauna (genus and species) at the province, county, district and village levels. Temporal distribution of sand flies was also recorded in the database at year and month levels, with the peak(s) of activity. Furthermore, Leishmania infection reports and susceptibility to insecticides were included, if available. Sticky paper traps were the most common method for sand fly collection in the reviewed studies, while other collection methods were CDC light traps, funnel traps, and hand catches using sucking tubes. The sand fly species identification was conducted using the taxonomic criteria, while the parasite species was identified based on isoenzyme analysis or PCR. The data were then transferred to ArcGIS9.3 to prepare the first spatial database of sand flies of Iran (we named it IrSandflybase). ArcMap was employed for mapping the distribution of vector species. Generic and subgeneric abbreviations were written based on the latest proposal in this field (Marcondes 2007).

The cutaneous type of leishmaniasis is endemic in more than half of the provinces and the main visceral foci are located in Ardabil (Northwest) and Fars (Southwest). There are also foci with low endemicity in other parts of the country (Fig 2). The IrSandflybase includes 131 papers (English and Persian languages), 2 abstracts and 71 MSc/PhD theses (Appendix table). This data base has 110,048 cells including different available data covering different aspects of ecology and biology of Iranian sand flies. Timeline of the published data was 1962–2012, although they reported the first study in 1930 (Mesghali, 1961). The following morphological keys were used for sand flies identification (Mesghali, 1961; Theodor and Mesghali, 1964; Nadim and Javadian, 1976; Seyedi-Rashti and Nadim, 1992). Based on the records of collection, temporal activity of sand flies in Iran is around 10 months in the warm regions of the southern part, while it may reduce to 7–8 months in central plateau or 4–5 months in cold areas of northwest (Fig. 3). During the active season, they have one (in northwest) or two (central plateau and south) peaks of activity. During May–September the climatic condition is favorable for breeding and activity of sand flies around the country, and null provinces in these months on the maps (Fig. 3) means there was no study in those areas. IrSandflybase includes 48 species in two genera of Phlebotomus and Sergentomyia. Each genus has 6 subgenera in Iran. The spatial distribution of sand flies is described below. 3.1. Phlebotomus This genus has 6 subgenera in Iran (Seyedi-Rashti and Nadim, 1992) as follows: • Subgenus Adlerius Nitzulescu, 1931 Based on the reviewed literature there are 7 species reported from this subgenus based on male specimens, because females cannot intensify with the available morphological keys. The reported species are: Phlebotomus balcanicus Theodor, 1958; Ph. brevis Theodor and Mesghali, 1964; Ph. halepensis Theodor, 1958; Ph. longiductus Parrot, 1928; Ph. salangensis Artemiev, 1978; Ph. turanicus Artemiev, 1974 and Ph. comatus Artemiev, 1978 (Theodor and Mesghali, 1964; Akhundi et al., 2012; Zahraei-Ramazani et al., 2013). • Subgenus Euphlebotomus Theodor, 1948 There are reports of two species in this subgenus in Iran: Phlebotomus ansarii Lewis, 1958 and Ph. eleanorae Sinton, 1931 (Seyedi-Rashti and Nadim, 1992). • Subgenus Larroussius Nitzulescu, 1931 Members of this subgenus are introduced as vectors of visceral leishmaniasis in Iran. There are 9 confirmed species as follows: Phlebotomus ilami Javadian, 1997; Ph. kandelakii Shchurenkova, 1929; Ph. keshishiani Shchurenkova, 1936; Ph. langeroni Nitzulescu, 1930; Ph. neglectus Tonnoir, 1921; Ph. perfiliewi transcaucasicus Parrot, 1930; Ph. smirnovi Perfil’ev, 1941; Ph. tobbi Adler and Theodor, 1930 and Ph. wenyoni Adler and Theodor, 1930 (Seyedi-Rashti and Nadim, 1992; Javadian et al., 1997; Naghian, 1997; YaghoobiErshadi, 2012). • Subgenus Paraphlebotomus Theodor, 1948

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Fig. 2. The mean incidence of cutaneous and visceral leishmaniasis in Iran, 2001–2011.

In this subgenus eight species including 2 subspecies are reported from different parts of the country including: Phlebotomus alexandri Sinton, 1928; Ph. andrejevi Shakirzyanova, 1953; Ph. caucasicus Marzinowsky, 1917; Ph. grimmi Porchinski, 1876; Ph. jacusieli Theodor, 1947; Ph. kazeruni Theodor and Mesghali, 1964; Ph. mongolensis Sinton, 1928; Ph. sergenti sergenti Parrot, 1917 and Ph. sergenti similis Perfil’ev, 1963 (Seyedi-Rashti and Nadim, 1992; Moin-Vaziri et al., 2007a,b; Yaghoobi-Ershadi, 2012). • Subgenus Phlebotomus Rondani and Brete, 1940 Three sand flies of this subgenus are reported from the country: Phlebotomus bergeroti Parrot, 1934; Ph. papatasi (Scopoli), 1786 and Ph. salehi Mesghali, 1965 (Seyedi-Rashti and Nadim, 1992). • Subgenus Synphlebotomus Theodor, 1948 There are reports of two species in this subgenus in Iran: Phlebotomus ansarii Lewis, 1958 and Ph. eleanorae Sinton, 1931 (Seyedi-Rashti and Nadim, 1992). 3.2. Sergentomyia This genus includes 6 subgenera in Iran (Theodor and Mesghali, 1964). They have no role in the transmission of leishmaniasis to humans, but introduced as vectors of lizard leishmaniasis. • Subgenus Grassomyia Theodor, 1958

• Subgenus Parvidens Theodor and Mesghali, 1964 It contains just one reported species in Iran: Se. iranica Lewis and Mesghali, 1961 (Lewis et al., 1961). • Subgenus Rondanomyia Theodor, 1958 Two species of sand flies were found in Iran related to this subgenus: Sergentomyia hodgsoni Sinton, 1933 and Se. pawlowskyi Perfil’ev, 1933 (Theodor and Mesghali, 1964). • Subgenus Sergentomyia Franca and Parrot, 1920 Up to now there are reports of five species of this subgenus in Iran: Sergentomyia antennata Newstead, 1912, Se. dentata Sinton, 1933; Se. mervynae Pringle, 1953, Se. sintoni Pringle, 1953 and Se. theodori Parrot, 1942 (Theodor and Mesghali, 1964; YaghoobiErshadi, 2012). • Subgenus Sintonius Nitzulescu, 1931 Three species from this subgenus are reported in Iran as follows: Sergentomyia christophersi Sinton, 1927; Se. clydei Sinton, 1928 and Se. tiberiadis Adler, Theodor and Lourie, 1930 (Theodor and Mesghali, 1964). 3.3. Spatial distribution of sand flies vectors of leishmaniasis in Iran

• Subgenus Parrotomyia Theodor, 1958

3.3.1. Cutaneous leishmaniasis (CL) Cutaneous leishmaniasis is the main vector-borne disease in the country with an average of more than 22,000 cases in the last decade (CDC, MoH, Iran, unpublished reports); about 80% of them are zoonotic cutaneous leishmaniasis (ZCL), The endemic foci of this type are in rural areas of 17 out of 31 provinces (Yaghoobi-Ershadi, 2012).

This subgenus contains six species in the country including: Sergentomyia africana Newstead, 1912; Se. baghdadis Adler and Theodor, 1929; Se. grekovi Khodukin, 1929; Se. palestinensis Adler and Theodor, 1927; Se. sogdiana Parrot, 1928 and Se. sumbarica Perfil’ev, 1933 (Theodor and Mesghali, 1964; Yaghoobi-Ershadi, 2012).

3.3.2. Zoonotic cutaneous leishmaniasis (ZCL) Based on the information of the IrSandflybase Phlebotomus papatasi is the main vector of ZCL, while Ph. salehi is also found to be infected with L. major in some foci of the diseases. Distribution maps show Ph. papatasi is reported from almost all studied areas of the

There are 2 species of sand flies from this subgenus in Iran as follows: Sergentomyia dreyfussi turkestanica Theodor and Mesghali, 1964 and Se. squamipleuris Newstead, 1912 (Theodor and Mesghali, 1964).

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Fig. 3. Observed monthly presence records of sand flies in different provinces of Iran up to 2012.

country (Fig. 4) and L. major and L. turanica were identified from this species (Yaghoobi-Ershadi et al., 1995; Rassi et al., 2011; YaghoobiErshadi, 2012). In all figures the green color shows no record/report of a sand fly species from those areas, yellow means report of collection and red color presents the counties where that sand fly species were found to be positive to the Leishmania parasite. Phlebotomus salehi is mainly reported in the southern part of the country (Fig. 4). The leptomonad infection of this sand fly, first reported from Sistan va Baluchestan (Kasiri and Javadian, 2000), is confirmed as L. major in Hormozgan and Fars province (Azizi et al., 2011, 2012;

Davami et al., 2011). Although leptomonad infection is observed in Ph. ansarii and Ph. caucasicus group, these species are known to have role in zoonotic cycle of CL between rodents (Yaghoobi-Ershadi and Javadian, 1996; Yaghoobi-Ershadi, 2012). 3.3.3. Anthroponotic cutaneous leishmaniasis (ACL) Phlebotomus sergenti s.l. is reported as the vector of ACL in Iran. It is found in 26 provinces of the country (Fig. 5). Three morphotypes of this sand fly were identified in the country by Moin-Vaziri et al. (2007a), and they reported Ph. sergenti similis for the first time. So

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Fig. 4. Presence of Ph. papatasi (left) and Ph. salehi (right) and their infection to Leishmania parasites in Iran at the county level up to 2012.

it is not clear that other reports of Ph. sergenti in Iran were due to which morphotype. Parasotilogical investigations have shown the infection of this sand fly to L. tropica (Oshaghi et al., 2010) and L. near gerbilii (Parvizi and Ready, 2008). 3.3.4. Visceral leishmaniasis (VL) Up to now 5 sand fly species are reported to be infected by leptomonad or were positive with PCR studies. The Larroussius subgenus with four positive species: Ph. neglectus (= Ph. major s.l.), Ph. kandelakii, Ph. keshishiani and Ph. perfiliewi transcaucasicus contains the probable vectors of VL in the country (Seyedi-Rashti et al., 1995; Azizi et al., 2008; Sanei Dehkordi et al., 2011; Rassi et al., 2012a). Infection of Ph. alexandri is also detected by PCR in southern foci of the disease (Azizi et al., 2006), and therefore this species is considered as a suspected vector in Iran. So we produced the distribution

Fig. 5. Presence of Ph. sergenti s.l. and its infection to Leishmania parasites in Iran at the county level up to 2012.

maps for these species (Fig. 6). There is also a report of infection of Ph. tobbi with L. infantum (Rassi et al., 2012b), but it needs more studies on the vectorial capacity of this species. Phlebotomus neglectus is almost reported in all cited references in the IrSandflybase as Ph. major, but Yaghoobi-Ershadi (2012) stated the specimens of Iran are Ph. neglectus. It has a wide distribution in the country (Fig. 6), and the infection of this species to L. infantum was reported from GhirKarzin area of Fars province (Azizi et al., 2008). Phlebotomus kandelakii was collected from west, northwest, some central areas and Kerman province as well as Khorassan-e-Razavi and Khorassan-e-Shomali provinces. The Leishmania infection of this species has been reported from Azarbaijan-e-Sahrghi province, northwest of Iran (Rassi et al., 2012a). Phlebotomus perfliewi is reported from west to northwest areas as well as Khorassan-e-Shomali and Chaharmahal va Bakhtiari provinces. There are some reports of infection of this sand fly to L. tropica, L. infantum and L. donovani in the country (Oshaghi et al., 2009a; Sanei Dehkordi et al., 2011). Phlebotomus keshishiani is distributed in Azarbaijan-e-Sharghi, Kordestan, Khuzestan, Bushehr, Fars, Hormozgan and Sistan va Baluchestan provinces. During a study in Ghirkarzin (Fars province), promastigotes of Leishmania parasite were found in some specimens and their injection to hamster resulted to the Leishmania infection (Seyedi-Rashti et al., 1995). Phlebotomus alexandri is reported in most studies on sand flies in the country. This species is found to be infected with L. infantum (Azizi et al., 2006). 3.3.5. Lizard leishmaniasis Lizard leishmaniasis is reported from some parts of the country, but because of low importance of this issue, there is no comprehensive study in this subject. This form of leishmaniasis, transmitted by Sergentomyia sand flies, is not infective for humans. By the way there are reports of infection in 3 sand fly species: Se. sintoni, Se. dentata and S. clyde. Sergentomyia sintoni is reported from all studied provinces of Iran (Fig. 7). The parasites detected in these sand flies are L. major, L. gymnodactyli and L. near gerbilli (Parvizi and Ready, 2008). Sergentomyia dentata is also collected from most studied areas. The infection of this species to L. adleri-like and L. tropica is reported in Ardabil and Azarbaijan-e-Sharghi provinces, respectively (Rassi et al., 1997, 2011; Oshaghi et al., 2009b). The third species, Se. clydei, is collected from some studied areas except for

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Fig. 6. Presence of suspected vectors of visceral leishmaniasis and their infection to Leishmania parasites in Iran at the county level up to 2012.

northwest of the country. This sand fly is found to be infeted in Lotfabad area, northeast of Iran and Baluchestan area, southeast (Seyedi-Rashti et al., 1971; Kassiri and Jahanifard, 2012). 4. Discussion It should be told that assess the validity and accuracy of the historical records is difficult, because diagnostic morphological

characters and species boundaries may be changed. For this reason the data was used for establishing IrSandflyBase that were published by known researchers in the field of sand fly studies. On the other hand suspected data were not used. Also the distribution maps of sand flies in this study were fitted based on the current boundaries at the county level. So, the names of villages/localities were considered, where a given species is reported. Then the current geographical situation of that locality was adjusted with

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Fig. 7. Presence of vectors of lizard leishmaniasis in Iran at the county level up to 2012.

the most recent administrative boundaries. Therefore, the presented maps show the spatial distributions at the existing counties, although they may be reported many years ago. Iran is located in Palearctic zone, although south of the country is located as the cross of three zones (Palearctic, Oriental and Afrotropical). So it is not surprising if species of three zones with different ecological requirement found in the country. Global warming and ecological changes caused by this issue will change the geographical distribution of sand fly species based on their biological needs. Comparing the current faunistic studies with old studies in the same area, indicated some species are new for the fauna of that area or disappeared. This may be partly due to climate change, although sampling methods can affect the issue. Therefore it is necessary for endemic countries to establish a database for vector-borne diseases, to map current distribution borders for the vector species, and to monitor their geographical distribution over the time (Galvez et al., 2011). SandflyMap is an online resource

presents a new service for sand flies around the world (Foley et al., 2012). This valuable resource needs for improvement by data from all countries. So our activity in establishing the IrSandflybase is a local effort with full details that can be shared with the global one. Furthermore using the current spatial distribution of sand flies in the country, it is possible to project the modeled distribution layer of the main vectors and use it for risk assessment of different type of leishmaniasis in the future. Ready (2013) has emphasized on the criteria for vector incriminating, proposed by Killick-Kendrick (1990). Based on these criteria, in addition to detecting Leishmania infection more than one occasion, it is necessary to find the infective form of the parasite in anterior midgut of the sand fly. Furthermore ecological association and human tendency, experimental transmission as well as using retrospective data for mathematical modeling can help to clear this issue. So it is recommended to say more cautiously about some newly infected species as vectors, because current studies

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are just based on typing the parasite. IrSandflybase now provides all available data for doing retrospective mathematical modeling of vectorial capacity of a given sand fly. Other benefit of this database is evaluation of taxonomic errors based on the geographical range of a given species, as we found some non-vector species out of their distribution range, surprisingly. Molecular taxonomy in recent years described some morphotypes for the Iranian sand flies (Badakhshan et al., 2011) and introduced even new species in some cases, such as Ph. sergenti similis and Ph. grimmi (Moin-Vaziri et al., 2007a,b). Based on the last published review on the fauna of Phlebotominae sand flies of Iran (Yaghoobi-Ershadi, 2012), there is doubt about existence of some previously reported species, because they did not confirm in the following studies. These species are: Ph. (Adl.) kabulensis Artemiev, 1978; Ph. (Adl.) salangensis Artemiev, 1978; Ph. (Adl.) turanicus Artemiev, 1974; Ph. (Eup.) caudatus Artemiev, 1978; Ph. (Lar.) langeroni Nilzulesco, 1930; Ph. (Lar.) smirnovi Perfiliew, 1941; Ph. (Tra.) mascittii Grassi, 1908 and Se. (Gras.) indica. Among these species, Ph. turanicus and Ph. salangensis are newly reported and described from northeast of Iran (Akhundi et al., 2012). Also Ph. smirnovi has been reported in 1995 from Azarbaijan-e-Gharbi (Naghian, 1997) and after that there is no more record of this species. A new report of Ph. (Adl.) comatus is described this species from northwest of the country (Zahraei-Ramazani et al., 2013). The last four mentioned sand flies were collected from the borderlines of Iran. Therefore, it seems that similarity of climate in these areas with the neighbor countries, where those mentioned species are reported, may be a reason for their occasionally collection. Also, changing the climate due to global warming and it’s ecological outcomes may affect the spatial distribution of different species and extend it inside the country (Cross et al., 1996; Cross and Hyams, 1996; Franke et al., 2002; Gonzalez et al., 2010). Phlebotomus turanicus introduced as vector of L. infantum in Turkmenistan (Lesnikova and Sabitov, 1995). This point is emphasized again on the distribution of the exotic vectors and the important role of an updated digital database for decision making in the control programs. Reports of some species like Ph. argentipes (Javadian and Mesghali, 1975), Ph. nuri, Ph. caudatus, Se. bailyi, Se. dolichopus and Se. adleri (Kasiri et al., 2000) are also found in the previous checklists of Iranian sand flies; among them only Ph. nuri is also collected from Baluchestan province of Pakistan (Kakarsulemankhel, 2004). So further studies are recommended to confirm occurrence of this species in Iran. Temporal distribution of sand flies in different Provinces, shows their activity is almost stopped in cold season, while during May–September there is at least one record of phlebotominae sand flies from almost all province, except for some provinces that there was no study till now. Therefore, during the fall season, the highland species such as Ph. kandelakii and Ph. perfiliewi transcaucasicus and some other vectors of visceral leishmaniasis are expected to be disappeared, while vectors of cutaneous leishmaniasis as well as lizard leishmaniasis that are mainly collecting in lowlands can be found in southern provinces. Finally, three key factors should be considered for recording of sand flies as well as other vectors: (a) It is suggested to whom is working in the field of sand flies to use a GPS device to record the exact coordinates of the collection sites, and put these coordinates in the faunistic reports. This issue will be an essential step for spatial studies that desire to predict the future distribution of different vector species under climate change scenarios. (b) It is recommended to confirm the identified species by the experts in the field of sand fly taxonomy (i.e. School of Public Health, Tehran University of Medical Sciences, Iran; or British Museum for new records/species).

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Spatial and temporal distributions of phlebotomine sand flies (Diptera: Psychodidae), vectors of leishmaniasis, in Iran.

Leishmaniasis is a major vector-borne disease and health problem in Iran. Studies on sand flies, as the vectors of the disease, began in the Northern ...
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