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Table of Contents
RESEARCH ARTICLE
Year : 2019  |  Volume : 56  |  Issue : 2  |  Page : 134-145

Annotated checklist of fleas (Insecta: Siphonaptera) and lice (Insecta: Anoplura) associated with rodents in Iran, with new reports of fleas and lice


1 Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran
2 Department of Entomology, Faculty of Agriculture and Natural Resources, Islamic Azad University, Arak, Iran

Date of Submission13-Jan-2018
Date of Acceptance25-Sep-2018
Date of Web Publication31-Jul-2019

Correspondence Address:
Kordiyeh Hamidi
Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-9062.263715

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  Abstract 

Background & objectives: Rodent species reported from Iran are subject of several studies, but the fauna called ectoparasite, infesting the rodents, along with their epidemic effects, are poorly known. In this study, ectoparasitic insect fauna of rodents found across the Iran were studied, to generate an annotated checklist of fleas and lice species.
Methods: Several field expeditions focused on different habitats of northeastern Iran were conducted between January 2017 and May 2018. Rodent trapping was carried out using custom-made mesh live traps and “Faragir” live traps baited mainly with scorched sunflower and gourd seeds. The trapped rodents were examined for ectoparasites on their body, and then released at their trapping point. The rodents and ectoparasite species were identified based on available keys.
Results: A total of 217 rodents belonging to 16 species of the families Calomyscidae, Cricetidae, Dipodidae, Mu- ridae and Sciuridae were captured. Five species of each fleas and lice were collected from the body of the trapped rodents. Three flea species, Ctenophthalmus pseudagyrtes, Nosopsyllus iranus and Xenopsylla buxtoni; and two louse species, Polyplax gerbilli and P. spinulosa, were recorded for the first time.
Interpretation & conclusion: The study generated an annotated checklist of 79 species of fleas and 8 species of lice harboured by different species of rodents distributed in Iran which would be helpful in different taxonomic studies such as parasite-host coevolution, and also sanitation and health monitoring programs.

Keywords: Fleas; Iran; lice; rodents; zoonotic disease


How to cite this article:
Hamidi K, Nassirkhani M. Annotated checklist of fleas (Insecta: Siphonaptera) and lice (Insecta: Anoplura) associated with rodents in Iran, with new reports of fleas and lice. J Vector Borne Dis 2019;56:134-45

How to cite this URL:
Hamidi K, Nassirkhani M. Annotated checklist of fleas (Insecta: Siphonaptera) and lice (Insecta: Anoplura) associated with rodents in Iran, with new reports of fleas and lice. J Vector Borne Dis [serial online] 2019 [cited 2019 Nov 17];56:134-45. Available from: http://www.jvbd.org/text.asp?2019/56/2/134/263715




  Introduction Top


Rodents are the most diverse mammalian groups which are found nearly in all habitats. Almost 73 rodent’s species have been recorded from Iran, of which about 31 species (belonging to seven families and 21 genera) are found in northeastern parts of Iran[1]. The important factors which seriously affect their distribution includes geographical varieties, climatic conditions, and ecological niches[1].

Most families of rodents are closely associated with ectoparasites and known as zoonotic reservoirs. More than 40 zoonotic diseases are known which can be transmitted by rodent hosts, e.g. plague, leptospirosis, salmo- nellosis, rat-bite fever, leishmaniasis, Chagas disease, Omsk hemorrhagic fever, bubonic plague, tularemia or Lyme disease, Lassa fever, murine typhus, etc[2].

Although, several publications have been reported on the ectoparasites of small mammals in Iran[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13], including distribution records of fleas and lice on rodents[4],[5],[6],[7],[11],[12],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29], but most of them focused on economically important species (mainly Rattus norvegicus, R. rattus, Mus musculus, Nesokia indica and Spermophilus fulvus) or reservoir hosts and/or vectors (especially Mu. musculus, R. norvegicus, Meriones libycus, Tatera indica, Rhombomys opimus) and were mainly in the form of case reports. However, comprehensive systematic studies on different ectoparasites of many other rodents are lacking.

The presence of a few taxonomic published data and lack of basic studies on rodent ectoparasites, the hae- matophagous insects, necessitates further such studies. Hence, this study aimed to generate an updated annotated checklist of fleas and lice species characterized from rodents, distributed in different areas of Iran, based on the original data and literature cited. This is the first checklist for the lice in Iran and the first comprehensive list for the fleas in Iran in the last 40 yr.


  Material & Methods Top


The field expeditions were carried out between January 2017 and May 2018 and rodent specimens were collected from North and South Khorasan provinces of Iran [Figure 1]. North Khorasan province covers an area of 28,434 km2 and has moderate mountainous climate. The average temperature of Bojnourd, the capital of North Khorasan, is 17.8 °C in spring, 23.2 °C in summer, 8.6 °C in fall, and 3.6 °C in winter. South Khorasan province covers an area of 95,385 km2 and has a semi-arid climatic condition in mountains and dry climate in plains and flat lands. The average temperature of Birjand, its capital city, is 21.9, 25.2, 11.3 and 7.5 °C in spring, summer, fall and winter, respectively.
Figure 1: Geographical location of North and South Khorasan provinces in northeastern and eastern Iran, respectively. Point localities of collected fleas and lice on their rodent’s hosts are shown in the map. Numbers in parentheses refer to the total frequencies of each ectoparasite species.

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Trapping was carried out in variety of habitats such as woodlands, meadows, sandy soils and rocky regions, deserts and semi-deserts, steppe regions, forests, parks, cultivated fields, farms and gardens spreading in Bojnourd, Faruj and Shirvan cities of North Khorasan province and Birjand, Ferdows, Nehbandan, Qaen and Sarayan cities of South Khorasan province throughout the year [Figure 1]. Custom-made mesh live traps and “Faragir” live traps baited mainly with scorched sunflower and gourd seeds were used for trapping[30].

The trapped rodents were examined for ectoparasites on their body in the field and then, released at their trapping point. The animals which were found dead in the traps, were transferred to the laboratory for further taxonomic studies on their skull and teeth. Collected ectoparasites were fixed in 70% alcohol. The fleas and lice specimens which were dark in colour were cleared by soaking in potassium hydroxide and treated with Nesbitt’s fluid. Subsequently, they were mounted on glass slides using Hoy er ‘s medium [Table 1]. Different determination keys were used for identification of rodents[31],[32], and ectoparasite species were identified based on keys which are available for Siphonaptera and Anoplura[33],[34],[35],[36]. Moreover, whole described species of fleas and lice were gathered by reviewing available published literature and were collated with the original data. Statistical descriptive analyses were performed via SPSS 16.0 (SPSS Inc. 2007).
Table 1: Total number of collected rodents (host), and fleas and lice reported to be harboured by them

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Ethical statement

Animal care was performed in compliance with the “Guidelines for the care and use of laboratory and experimental animals”, Rodentology Research Group, Fer- dowsi University of Mashhad[37].


  Results Top


In the present study, a total of 217 rodents collected from eight different localities in North and South Khorasan provinces, in northeastern and eastern Iran, re-spectively were examined for infestation; which included species—Calomyscus elburzensis Goodwin 1938, and Ca. hotsoni Thomas 1920 (Family: Calomyscidae); Cri-cetulus migratorius (Pallas 1773), Ellobius fuscocapillus Blyth 1843, and Microtus paradoxus Ognev et Heptner 1928 (Family: Cricetidae); Scarturus elater (Lichtenstein 1828) (Family: Dipodidae); Meriones libycus Lichtenstein 1828, M. persicus (Blanford 1875), Rhombomys opimus (Lichtenstein 1828), Tatera indica (Hardwicke 1807), Apodemus witherbeyi (Thomas 1902), Mu. musculus Linnaeus 1758, Nesokia indica (Gray 1830), Rattus norvegicus (Berkenhout 1769), and R. pyctoris Hodgson 1845 (Family: Muridae); and Spermophilus fulvus Cuvier 1825 (Family: Sciuridae).

Five species of fleas, namely Ctenophthalmus pseu-dagyrtes Baker 1904, Nosopsyllus fasciatus (Bosc 1801), N. iranus Wagner and Argyropulo 1934, Xenopsylla bux-toni Jordan 1949 and X. cheopis (Rothschild 1903); and five species of lice comprising Hoplopleura captiosa Johnson 1960 Polyplax asiatica Ferris 1923, P. gerbilli Ferris 1923, P.paradoxa (Johnson 1960), and P. spinulosa (Burmeister 1839) were observed. Three flea species, Ct. pseudagyrtes, N. iranus and X. buxtoni, and two lice species, P. gerbilli and P. spinulosa, were recorded for the first time from rodents found in northeastern and eastern Iran.

Information about the capturing localities in which each ectoparasite species was found on its rodent host, and the number of collected ectoparasites are shown in [Figure 1]. The total number of each trapped rodent hosts, as well as collected fleas and lice are given in [Table 1].

Notes on checklist

The following list describes the principal hosts for each ectoparasite species, along with brief information about their significant records and medical importance (where available). All taxa (fleas and lice) are arranged alphabetically. An asterisk (*) preceding an entry indicates that the mentioned species is identified during the present study.



Part I: List of fleas and their principal hosts

Order: Siphonaptera Latreille 1825 Family: Ceratophyllidae Dampf 1908 Genus: Callopsylla Wagner 1934 – Callopsylla saxatilis (Ioff et Argyropulo 1934): On Microtus nivalis[19] Genus: Citellophilus Wagner 1934

– Citellophilus trispinus (Wagner et Ioff 1926): On S. fulvus[19]

Genus: Ctenophthalmus Kolenati 1856

– Ctenophthalmus pseudagyrtes* Baker 1904: On R. norvegicus, with no definite indication on flea spe- cies[5],[6],[25]. Rattus norvegicus has been previously reported by Hamidi et al[6] as a host rodent for this species in Iran. Rattus norvegicus collected from Faruj showed infestation with Ct. pseudagyrtes.



Genus: Myoxopsylla Wagner 1927

– Myoxopsylla jordani Ioff et Argyropulo 1934: On Dryomys nitedula[19]

Genus: Nosopsyllus Jordan 1933

– Nosopsyllus baltazardi Farhang-Azad 1970: On Ger- billus cheesmani, G. nanus, M. crassus, M. libycus, M. persicus, Rh. opimus and T. indica[19]

– Nosopsyllus consimilis (Wagner 1898): On Microtus socialis[21]

– Nosopsyllus fasciatus* (Bosc 1801): On Apodemus sylvaticus, M. persicus, Mi. socialis, Mu. musculus, R. norvegicus, Arvicola terrestris, Nesrokia indica, Spermophilus fulvus[5],[6],[9],[12],[25],[26],[27], Scarturus williamsi, Cricetutus migratorius, Mesocricetus auratus and R. rattus[19],[39],[40]. This species has been previously recorded on Ne. indica and S. fulvus[6].

In this study, N. faciatus was found on Mi. paradoxus captured from Shirvan, M. libycus from Shirvan and Nehbandan,M. persicus from Faruj, Bojnourd, Sarayan, Ferdows and Nehbandan, Rh. opimus from Bojnourd, Mu. musculus from Biijand, Ne. indica from Shirvan and S. fulvus from Bojnourd.

– Nosopsyllus farahae Farhang-Azad 1973: On Mi. socialis[35]

– Nosopsyllusfidus (Jordan et Rothschild 1915): On Ger- billus nanus[35]

– Nosopsyllus iranus* Wagner and Argyropulo 1934: On Cr. migratorius and Mu. musculus[12], M. libycus, M. tristrami, M. vinogradovi, Mi. irani, Mi. socialis and R. norvegicus[22],[26].

This species was collected from the body of Ca. elburzensis from Bojnourd, Cr. migratorius from Shirvan, M. persicus from Shirvan, Bojnourd, Qaen, Biijand, Sarayan and from Mu. musculus from Bojnourd and Shirvan.



– Nosopsyllus laeviceps (Wagner 1909): On M. libycus, M. persicus, Mi. socialis, Jaculus blanfordi and Rh. opimus[11],[19],[40]

– Nosopsyllus londiniensis (Rothschild 1903): On Mu. musculus[19]

– Nosopsyllus medus Jordan 1938: On Mu. musculus[19],[40]. Telmadarraiy et al[29] have reported the presence of this species on rodents, with no definite indication on host species.

– Nosopsyllus mikulini (Kunitsky et Kynitskaya 1961): On Cr. migratorius, M. libycus, M. persicus, M. vino- gradovi, Me. auratus, Mi. arvalis, Mi. irani, Mi. socialis, Mu. musculus and R. norvegicus[19],[40]

– Nosopsyllus mokrzeckyi (Wagner 1916): On Cr. migratorius and Mi. socialis[19]

– Nosopsyllus monstrosus (Wagner 1928): On Rh. opimus[42]

– Nosopsyllus philippovi (Zagniborodova et Mikulin 1957): On Calomyscus bailwardi, E. fuscocapillus, Mi. arvalis, Mi. socialis and Mu. musculus[19]

– Nosopsyllus pringlei Hubbard 1956: On Gerbillus nanus, Jaculus jaculus, J. blanfordi, M. crassus, M. libycus, M. persicus, Rh. opimus and T. indica[17],[19],[40]

– Nosopsyllus sarinus (Jordan et Rothschild 1921): On M. persicus, Mu. musculus and R. norvegi- cus[19],[40],[42],[43]

– Nosopsyllus tersus (Jordan et Rothschild 1915): On Rh. opimus[19]

– Nosopsyllus turkmenicus (Vlasov et Ioff 1937): On Cr. migratorius, G. nanus, M. persicus, M. libycus and Rh. opimus[19]

– Nosopsyllus vlasovi (Vlasov et Ioff 1937): On M. crassus, M. libycus, M. meridianus and Rh. opimus[19]



Family: Coptopsyllidae Wagner 1928 Genus: Coptopsylla Jordan and Rothschild 1908

– Coptopsylla bairamaliensis Wagner 1928: On M. persicus and Rh. opimus[15],[16],[19],[20]

– Coptopsylla iranica Farhang-Azad 1966: On G. nanus, M. crassus, M. libycus, M. meridianus and M.persicus[16],[20]

– Coptopsylla lamellifer (Wagner 1895): On M. libycus, M. persicus, M. vinogradovi and Rh. opimus[15],[19],[20]

– Coptopsylla mofidii Farhang-Azad 1966: On Ca. bailwardi, Cr. migratorius, G. nanus, M. crassus, M. libycus, M. persicus, Rh. opimus and T. indica[16],[19],[20]

– Coptopsylla neronovi Farhang-Azad 1972: On M. crassus and M. persicus[20]

– Coptopsylla sp.: On Mu. musculus[14]



Family: Ctenophthalmidae Rothschild 1915 Genus: Ctenophthalmus Kolenati 1856

– Ctenophthalmus congener Rothschild 1907: On A. sylvaticus, M. persicus, Mi. arvalis and Mi.

socialis[19],[20]

– Ctenophthalmus dolichus Rothschild 1913: On Cr. migratorius, M. libycus, M. persicus and M. vinogra-dovi[19],[40]

– Ctenophthalmus iranus Argyropulo 1935: On Cr. migratorius, Me. auratus, M. libycus, M. persicus, M. tristrami, M. vinogradovi, Mi. irani, Mu. musculus and Ne. indica[19],[40],[43]

– Ctenophthalmus proximus (Wagner 1903): On A. syl-vaticus[42]

– Ctenophthalmus rettigi Rothschild 1908: On Sc. wil-liamsi and Me. auratus[19],[40]

Genus: Neopsylla Wagner 1903

– Neopsylla pleskei Ioff 1928: On M. persicus and S. fulvus[19],[40]

– Neopsylla setosa (Wagner 1898): On Cr. migratorius and S. fulvus[19]

– Neopsylla teratura Rothschild 1913: On Cr. migratorius[19],[40]

Genus: Rhadinopsylla Jordan and Rothschild 1912

– Rhadinopsylla bivirgis Rothschild 1913: OnM. libycus and M. persicus[19]

– Rhadinopsylla syriaca Lewis 1962: OnM. libycus[19]

– Rhadinopsylla ucrainica Wagner et Argyropulo 1934: On Cr. migratorius, M. libycus, M. persicus, M. tristrami, M. vinogradovi, Me. auratus, Mi. irani, Mi. socialis and Mu. musculus[19]

Genus: Stenoponia Jordan and Rothschild 1911

– Stenoponia tripectinata (Tiraboschi 1902): On Ca. bailwardi, G. nanus, M. crassus, M. libycus, M. persi-cus, M. tristrami, M. vinogradovi, Rh. opimus, S. fulvus and T. indica[19]

– Stenoponia vlasovi Ioff et Tiflov 1934: OnM. persicus and Rh. opimus[17],[19]

Genus: Wagnerina Ioff et Argyropulo 1934

– Wagnerina schelkovnikovi Ioff et Argyropulo 1934: On Ca. bailwardi, Cr. migratorius, M. persicus, Me. auratus, Mu. musculus and Ne. indica[19]

Family: Leptopsyllidae Baker 1905

Genus: Amphipsylla Wagner 1909

– Amphipsylla argoi Ioff 1946: On Ca. bailwardi[19]

– Amphipsylla parthiana Ioff 1950: On Mi. arvalis and Mi. socialis[19]

– Amphipsylla rossica Wagner 1912: On Mi. irani[19]

– Amphipsylla schelkovnikovi Wagner 1909: On Cr. migratorius, M. libycus, M. persicus, M. vinogra- dovi, Me. auratus, Mi. irani, Mu. musculus and R. norvegicus[19]

Genus: Caenopsylla Rothschild 1909

– Caenopsylla laptevi Mikulin et Zagniborodova 1958: On T. indica[11],[19]

Genus: Frontopsylla Wagner and Ioff 1926

– Frontopsylla ambigua Fedina 1946: On Ca. bailwardi[19]

Genus: Leptopsylla Jordan and Rothschild 1911

– Leptopsylla aethiopicus Jordan and Rothschild 1911: On Mu. musculus[44]



– Leptopsylla segnis (Schonherr 1811): On Mu. muscu-lus, R. norvegicus and R. rattus[19]

– Leptopsylla taschenbergi (Wagner 1898): On A. syl-vaticus, Mu. musculus and R. rattus[19],[45]

Genus: Mesopsylla Dampf 1910

– Mesopsylla eucta Dampf 1910: On Sc. elater, Sc. williamsi, Cr. migratorius, M. libycus, M. persicus, M. tristrami and M. vinogradovi[19]

– Mesopsylla tuschkan Wagner et Ioff 1926: On Sc. elater and Sc. williamsi[19]

Genus: Ophthalmopsylla Wagner and Ioff 1926

– Ophthalmopsylla volgensis (Wagner et Ioff 1926): On Sc. elater, Sc. williamsi, Cr. migratorius, M. libycus, M. persicus and M. vinogradovi[19]

Genus: Paradoxopsyllus Miyajima and Koidsumi 1909

– Paradoxopsyllus faghohei Farhang-Azad 1972: On Calomyscus sp.[26]

– Paradoxopsyllus grenieri Klein 1963: On M. persicus and M. vinogradovi[19]

– Paradoxopsyllus microphthalmus Ioff 1946: On Ca. bailwardi and M. persicus[19],[40]

Genus: Peromyscopsylla Fox 1939

– Peromyscopsylla tikhomirovae (Ioff 1946): On Ca. bailwardi and M. persicus[19]

Genus: Phaenopsylla Jordan 1915

– Phaenopsylla newelli Farhang-Azad 1972: On Calo- myscus sp.[22]

– Phaenopsylla kopetdag Ioff1946: On Ca. bailwardi[22]

– Phaenopsylla tiflovi Ioff 1950: On Ca. bailwardi[19]

Family: Pulicidae Billberg 1820

Genus: Ctenocephalides Stiles and Collins 1930

– Ctenocephalides canis (Curtis 1826): On T. indica[19]

– Ctenocephalides felis (Bouche 1835): On R. norvegicus[19]

– Ctenocephalides orientis (Jordan 1925): On R. rattus[19] Genus: Echidnophaga Olliff 1886

– Echidnophaga oschanini Wagner 1930: On M. libycus, M. persicus and Rh. opimus[17],[19]

Genus: Parapulex Wagner 1910

– Parapulex chephrenis (Rothschild 1903): On Acomys sp.[19]

Genus: Pulex Linnaeus 1758

– Pulex irritans Linnaeus 1758: On rodents[29]



Genus: Synosternus Jordan 1925

– Synosternus cleopatrae (Rothschild 1903): On G. cheesmani, G. nanus and T. indica[19]

– Synosternus pallidus (Taschenberg 1880): On T. indica[19]

Genus: Xenopsylla Glinkiewicz 1907

– Xenopsylla astia Rothschild 1911: On Acomys dimidi-atus, Ca. bailwardi, J. jaculus, M. crassus, M. hurri-anae, Mu. musculus, Ne. indica, R. norvegicus, R. rattus, S. fulvus and T. indica[19],[24],[28]



– Xenopsylla buxtoni* Jordan 1949: On A. sylvaticus, Ca. bailwardi, Cr. migratorius, M. persicus, Mi. socialis and R. rattus[12], R. norvegicus and T. indica[1] and generally on many other rodents[29]. This species has also been reported from Sc. elater, Sc. williamsi, Cr. migratorius, M. libycus, M. tristrami, M. vinogradovi, Me. auratus, Mi. arvalis, Mi. irani, Mi. socialis, Mu. musculus and Ne. indica[7],[17],[19],[28],[29],[39]. This species was collected from M. persicus found in Nehbandan, R. norvegicus found in Faruj and R. pyctoris found in Shirvan.

– Xenopsylla cheopis* (Rothschild 1903): On R. norvegicus and R. rattus[24], M. persicus and Ne. indica[5],[6],[25],[28], also on Cr. migratorius, M. persicus, Mu. musculus and S. fulvus[19],[28]. Hamidi et al[6] reported that the species M. persicus and Ne. indica are the hosts of X. cheopis. This species is also found onM. persicus and Ne. indica collected from Shirvan and Ferdows Cities, and also on R. norvegicus collected from Bojnourd City.



– Xenopsylla conformis (Rothschild 1904): On Sc. elater, Ca. bailwardi, Cr. migratorius, G. nanus, J. blanfordi, J. jaculus, M. crassus, M. libycus, M. meridianus, M. persicus, M. vinogradovi, M. tristrami, Ne. indica, Rh. opimus, S. fulvus and T. indica[17],[19],[28],[39],[40]



– Xenopsylla gerbilli (Wagner 1903): On Rh. opimus[19]

– Xenopsylla hussaini Sharif 1930: On G. cheesmani, G. nanus, M. persicus, Ne. indica and T. indica[19]

– Xenopsylla hutoni (Rothschild 1904): On rodents[28]

– Xenopsylla nubica (Rothschild 1903): On Sc. elater, J. blanfordi and J. jaculus[17],[19],[28],[39]

– Xenopsylla nuttalli (Ioff 1930): On Ca. bailwardi, E. fuscocapillus, G. cheesmani, G. nanus, H. indica, M. crassus, M. meridianus, M. persicus, Ne. indica, Mu. musculus, Rh. opimus and T. indica[17],[19]

– Xenopsylla persica (Ioff 1946): On M. persicus and Rh. opimus[19]



Part II: List of lice and their principal hosts

Order: Anoplura Leach 1815 Family: Hoplopleuridae Ewing 1929 Genus: Hoplopleura Enderlein 1904

– Hoplopleura captiosa * Johnson 1960: On R. norvegicus[1] and Ne. indica[6]. It was found on Mu. musculus collected from Shirvan and R. norvegicus collected from Faruj.





– Hoplopleura oenomydis Ferris 1921: On R. nor-vegicus[9].– Hoplopleura sp: On R. norvegicus[9], Ar. terre stris, Ne. indica and R. rattus[26],[27].



Family: Polyplacidae Fahrenholz 1912 Genus: Linognathoides Cummings 1914 – Linognathoides laeviusculus (Grube 1851): On A. syl-vaticus, M. persicus and Mi. socialis[12].



Genus: Polyplax Enderlein 1904

– Polyplax asiatica* Ferris 1923: On M. persicus and Ne. indica[5],[6],[25]. This species has been reported as an ectoparasite of M. persicus[6]. In addition, Ne. indica collected from Shirvan and Cr. migratorius collected from Bojnourd hosted this species.



– Polyplax gerbilli* Ferris 1923: On R. norvegicus and T. indica[7]. This species was found on the body of T. indica and R. norvegicus from Faruj.



– Polyplax paradoxa* (Johnson 1960): On M. persicus[5],[6],[25], also on M. persicus collected from Shirvan, Sarayan and Qaen were infested with P. paradoxa.





– Polyplax spinulosa* (Burmeister 1839): On A. sylvati-cus and R. norvegicus[9] and other rodents[24],[28],[29]. This species was collected from R. norvegicus captured from Faruj.



Short descriptions and medical hazards

Diagnostic morphological characteristics [Figure 2], [Figure 3], [Figure 4], [Figure 5] and some notes on medical importance of two most common fleas (N. fasciatus and X. cheopis) and two lice (H. captiosa and P. spinulosa) species are given below:
Figure 2: Key identification characteristics of Nosopsyllus fasciatus (Male).

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Figure 3: Key identification characteristics of Xenopsylla cheopis (Male).

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Figure 4: Key identification characteristics of Hoplopleura captiosa (Male or Female).

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Figure 5: Key identification characteristics of Polyplax spinulosa (Male or Female).

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Family: Ceratophyllidae

Outer internal ridge of midcoxa present; pronotum with a course of pigmented spines; without rod-like link between based abdominal sternum and wetepimeron; metanotum with marginal spinelets seusilium flatin (females); genal comb (row of strong bristles) may be present/absent, but never consist spines near oral angle; tento-rial arch absent, three bristles in outer row, upper bristle is in front of eyes, and sternum VIII of males reduced or vestigial.

Genus: Nosopsyllus

These fleas are recognized/distinguished from the other medically important genera by the presence of a pronotal comb, a mesopleural rod and a well-developed pleural arch (located between the third thoracic segment and the abdomen); large eye; femur I with a number of lateral setae; inner surface of coxae II and III with fine setae; vestigial sternum VIII in males; movable finger; longer slender setae, and globular head of spermatheca.

Species: Nosopsyllus fasciatus

Labial palpus short, not extending to tip of coxa of first leg; pronotal comb present; two rows of bristles on typical abdominal segment; labial palps not extending beyond trochanter of first pair of legs; segments V of hind tarsi with five pairs lateral plantor bristles; process of clasper broad, the two sides meeting the truncate apex at about 90° angles, and sternite VII of females almost straight [Figure 2].



Family: Pulicidae

Outer internal ridge of mid-coxa absent; inner side of hind coxa with spiniform bristles; abdominal terga II-VI with a single row of bristles; with two well-developed compound eyes; with or without genal comb.

Genus: Xenopsylla

Comb of genal spines absent (a single genal spine may be present); anterior margin of head rounded; pleural rod of mesothorax present.

Species: Xenopsylla cheopis

Genal and pronatal combs absent; front margin of head rounded (three thoracic tergites together longer than the first abdominal tergite); thorax normal (not contracted); mesopleuron divide by vertical rod-likes thickening (rod-like sclerotization); ocular bristle inserted in front of eye; one row of bristles on typical abdominal segment, and female with spermatheca partially pigmented [Figure 3].



Family: Hoplopleuridae

Abdomen with poorly defined plates or without plates; abdomen without spiracles or parallel rows of setae (nym-phus); lateral plates large, and emarginated posteriorly, and segment II of antenna longer than wide.

Genus: Hoplopleura

Paratergites of abdominal segments III–V bilobate; paratergite of abdominal segment III with one short apical seta or a pair of long setae; paratergite of abdominal segments VII–VIII with or without distinct apical lobe; Sternal plate II not divided medially; thoracic sternal plate heart-shaped with a rounded anterior process or not heart-shaped but with short anterior and long posterior processes; abdominal spiracles small to unusually large, and diameter < 0.020 to > 0.030 mm.

Species: Hoplopleura captiosa

Head and thorax with only a few setae; without eyes or occular points; parategral plates on at least one abdominal segment usually as long as, or at least as long as the sternal plate; first pair of legs smallest; the second pair with stouter claws than others; abdomen with lateral plates; two groups of 2 or 3 stout spines present at the base of the abdomen; antennae fire-segmented; third leg without bladder-like expansions; first sternite of abdominal segments extended laterally to articulate with its corresponding paratergal plate, and abdominal sternite I with two groups of 2 or 3 stout setae [Figure 4].



Family: Polyplacidae

Abdomen with poorly defined plates or without plates; abdomen without spiracles or parallel rows of setae (nymphus); lateral plates small, and segment II of antenna as long as wide.

Genus: Polyplax

Sternal plate of thorax usually pointed posteriorly or if truncated, always associated with a huge enlargement of the first antennal segment; abdomen with well-defined ventral, lateral and dorsal plates; lateral plates small, sub-triangular; segment II of antenna as long as wide; without eyes or ocular points; abdomen with lateral plates, and front of sternal plate not rounded.

Species: Polyplax spinulosa

Rounded head with two five-segmented antennae; ventral thoracic plate with pentagonal shape; abdomen with about seven lateral plates on each side and 7–13 dorsal plates; third segment of the male antennae provided with a pointed apophysis; paratergal plate IV with short or subequal setae, and paratergal plates III–V with only dorsal apical reduced angle produced into a point [Figure 5].

The spined rat louse, P. spinulosa, is a blood sucking louse which has been reported as a biological vector of a number of infectious agents (bacteria, viruses, and several protozoan species). Clinical signs of heavy infestation include anaemia, dermatitis, unthrifty appearance, scratching, and small skin wounds. In addition, it may serve as a vector of Mycoplasma sp. (chronic respiratory disease: CRD), R. typhi (murine/endemic typhus), Trypanosome sp. (human African trypanosomiasis, also known as sleeping sickness), Borrellia sp. (borreliosis) and Brucella sp. (brucellosis)[54].


  Discussion Top


Most of rodents are considered as possible reservoirs for different zoonotic diseases. They can carry serious pathogens (bacteria, viruses, fungi and parasites) that cause infectious diseases in humans which range from commonly fatal (such as bubonic plague and rabies), to the relatively trivial or with low fatality rate (e.g. skin mange or salmonellosis). These infectious pathogens/agents can be carried by arthropods/ectoparasites (fleas, lice, mites, ticks, flies) or may show direct transmission from animals to humans (mainly in the case of viral diseases such as hantaviruses). Wide range of zoonotic diseases is spread by the infected droppings and urine of small mammals, mainly rodents[6],[55]. Hence, identification of ectoparasitic fauna of rodents is very important in the way to conquer this great concern.

In the present study, several rodent’s species were collected from two provinces in the northeast and eastern Iran. Results showed that the most common trapped rodent belongs to the species Mu. musculus (17.05%) and the least captured is R. pyctoris (0.46%). The examined fleas during this study belonged to two families (Cera-tophyllidae and Pulicidae). Spermophilus fulvus was the most prevalent rodent infested by these fleas (on average 3.8 fleas per host individual) and Rh. opimus with on average 0.3 fleas per host individual showed the lowest flea infestation. Furthermore, several louse species belonging to families Hoplopleuridae and Polyplacidae were recorded during the field expeditions. Rattus norvegicus and T. indica showed highest (on average 1.6 lice per host individuals) and lowest (on average 0.3 lice per host individuals) infestation by lice, respectively. These results revealed that harbouring of fleas is more common than lice (more than twice) in rodents distributed in northeast and eastern Iran which is in accordance with author’s previous study. According to Moravvej et al (2016)[25], the prevalence rate reported for rodent’s infestation by fleas and lice in Razavi Khorasan province was 44.57 and 24.09%, respectively.

The three species of fleas (Ct. pseudagyrtes, N. iranus and X. buxtoni) and two species of lice (P. gerbilli and P. spinulosa) are recorded for the first time from rodents distributed in the east and northeastern parts of Iran.

The east of Iran is the point of direct contact between two cradles of endemism, northeastern Iran and Turkmenistan[56]. Topographic situation and climatic conditions play an important role in distribution of rodents in this area and consequently their ectoparasitic fauna. The associations of rodents and their ectoparasites with human habitation, as well as host-ectoparasite coevolution and the role of rodents and their ectoparasites affinity in the life cycle of emerging new infections, are considered as important issues in epidemiological and zoonotic investigations[5],[6],[25].

Transferring of pathogens between species (animals and humans) and spreading zoonotic diseases to new areas simply occurs via moving the animals from one place to another, e.g. for feeding or nesting. In these conditions, the infection may pass to other animals or may be acquired by human with direct or indirect contact to animals. Poor living conditions precipitate the outbreak of pathogens of human health importance carried by infected animals. To overcome these problems, increasing the knowledge on rodent’s distribution pattern and population structure as well as their associated parasites, the way of dealing with the probable pathogen, eliminating them early and promptly and also preventing the entry of most pathogens into human facilities through health monitoring programs, are among important efforts in preventing zoonoses emergence and development[57]. Most of the species of Anoplura (about 71%) which have been currently described are collected from rodent’s body[53]. Understanding the diversity of ectoparasite species harbouring rodents would provide valuable insights into their roles in the control of host populations. For example, sucking lice are widely distributed around the world and generally considered as highly host- specific parasite, for major groups of eutherian mammals.


  Conclusion Top


Based on the original data of this study and its collation with related published records, an annotated checklist of 79 species of fleas and 8 species of lice harboured by different species of rodents in Iran was generated, which would be helpful in different taxonomic studies such as parasite-host coevolution, and also sanitation and health monitoring programs. There are several difficulties in finding some of the small-sized ectoparasites such as lice and mites on rodent’s body and/or between their hair, as compared with collecting large ectoparasites (e.g. fleas and ticks); which subsequently makes their identification more difficult. Further taxonomic studies focused on the estimation of diversity of such small ectoparasites are therefore necessary for accurate estimation of their prevalence in the rodents and prevention of disease transmission. Monitoring the rodent’s population and their ectoparasites is recommended to ascertain the role of rodents in the life cycle of emerging new infestations in Iran.

Conflict of interest

The authors declare that they have no competing interest.


  Acknowledgements Top


The authors wish to express their sincere thanks to H. Mozaffari and A. Hamidi for their financial support and kind assistance in the field studies and capturing rodents. Thanks are also due to Dr A.M. Benedek and S. Mohammadi, and also annonymous reviewers for their critical review of the manuscript which greatly improved the content.



 
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