The Fleas (Siphonaptera) in Iran: Diversity, Host Range, and Medical Importance.

BACKGROUND: Flea-borne diseases have a wide distribution in the world. Studies on the identity, abundance, distribution and seasonality of the potential vectors of pathogenic agents (e.g. Yersinia pestis, Francisella tularensis, and Rickettsia felis) are necessary tools for controlling and preventing such diseases outbreaks. The improvements of diagnostic tools are partly responsible for an easier detection of otherwise unnoticed agents in the ectoparasitic fauna and as such a good taxonomical knowledge of the potential vectors is crucial. The aims of this study were to make an exhaustive inventory of the literature on the fleas (Siphonaptera) and range of associated hosts in Iran, present their known distribution, and discuss their medical importance. METHODOLOGY/PRINCIPAL
FINDINGS: The data were obtained by an extensive literature review related to medically significant fleas in Iran published before 31st August 2016. The flea-host specificity was then determined using a family and subfamily-oriented criteria to further realize and quantify the shared and exclusive vertebrate hosts of fleas among Iran fleas. The locations sampled and reported in the literature were primarily from human habitation, livestock farms, poultry, and rodents' burrows of the 31 provinces of the country. The flea fauna were dominated by seven families, namely the Ceratophyllidae, Leptopsyllidae, Pulicidae, Ctenophthalmidae, Coptopsyllidae, Ischnopsyllidae and Vermipsyllidae. The hosts associated with Iran fleas ranged from the small and large mammals to the birds. Pulicidae were associated with 73% (56/77) of identified host species. Flea-host association analysis indicates that rodents are the common hosts of 5 flea families but some sampling bias results in the reduced number of bird host sampled. Analyses of flea-host relationships at the subfamily level showed that most vertebrates hosted fleas belgonging to 3 subfamilies namely Xenopsyllinae (n = 43), Ctenophthalminae (n = 20) and Amphipsyllinae (n = 17). Meriones persicus was infested by 11 flea subfamilies in the arid, rocky, mountainous regions and Xenopsyllinae were hosted by at least 43 mammal species. These findings place the Persian jird (M. persicus) and the Xenopsyllinae as the major vertebrate and vector hosts of flea-borne diseases in Iran including Yersinia pestis, the etiological agent of plague. We found records of at least seven vector-borne pathogenic agents that can potentially be transmitted by the 117 flea species (or subspecies) of Iran.
CONCLUSIONS/SIGNIFICANCE: Herein, we performed a thorough inventary of the flea species and their associated hosts, their medical importance and geographic distribution throughout Iran. This exercise allowed assessing the diversity of flea species with the potential flea-borne agents transmission risk in the country by arranging published data on flea-host associations. This information is a first step for issuing public health policies and rodent-flea control campaigns in Iran as well as those interested in the ecology/epidemiology of flea-borne disease.

Introduction

Vector-borne diseases (VBDs) are globally responsible for more than 17% of all infectious diseases [1]. There are a large number of viral, rickettsial, bacterial and parasitic diseases that are transmitted by insect vectors [2]. In the last two decades, many zoonotic VBDs have emerged in areas where they previously did not occur, and the incidence of these diseases both in endemic areas and outside their known range has increased [3]. In recent years, most studies on zoonotic diseases have focused on tick- and mosquito-borne diseases, less attention has been given to flea-borne diseases[4].

Fleas (Siphonaptera) are small, bloodsucking or hematophagous ectoparasites that may transmit pathogens through several possible mechanisms, including: contaminated feces (e.g. R. typhi, B. henselae), soiled mouthparts (e.g. Y. pestis, viral pathogens), regurgitation of gut contents (e.g. Y. pestis), and infectious saliva (e.g. R. felis in salivary glands)[4].

Over 2500 flea species belonging to 16 families and 238 genera have been described worldwide [5]. Fleas are mainly ectoparasites of mammals while birds are infested by only 6% of the known species. This is partly due to reduced collection efforts and sampling bias as only few bird fleas are in close contact with humans [6]. Fleas are one of the most common insect groups that can serve as vector and intermediate host of pathogenic zoonotic agents between vertebrate hosts, including humans [4, 7–8]. Fleas can have a direct pathogenic effect by causing allergic dermatitis [9-10] or paralysis subsequent to the injection of saliva into their hosts skin or blood [11]. Notorious human pathogens such as Yersinia pestis (plague), Rickettsia typhi (murine typhus), Francisella tularensis (tularemia) and Bartonella henselae (cat scratch disease) are transmitted by fleas [12-15].

Some fleas tend to be host specific (restricted or specialist), but others have a wide host range (permissive, opportunistic). The permissive species group are more significant than the restricted ones, because they can spread infectious agents among and within their multiple hosts and across a diverse series of habitats [6]. In order to prevent or control the occurrence and spread of flea-borne diseases, it is thus necessary to establish a taxonomical inventory of the flea fauna and their specific distribution range.

Climate changes, due to global warming and human intervention, have led to changes in the biological parameters and distribution ranges of vectors and hence of VBDs [16]. On the bases of vulnerability assessments and models, it is predicted that climate change will result in raised incidence of communicable diseases embracing VBDs; however the short and long term effects will be mitigated and will be linked to vector life cycles (e.g.: developments of preimaginal stages) and geographic area [17]. Reasonable proofs tend to suggest that changes in climatic factors may affect VBDs incidence especially acting on the off-host developmental life stages of arthropods and hence disease transmission dynamics. Insects as poikilotherm organisms have no internal control of their body temperatures, and as such depend on their host(s)—the imago as a transient habitat -, and abiotic conditions for survival, which both condition their vector capacity, as well as their reproduction rate[18]. Moreover, vector capacity is linked to the nature of the pathogen transmitted, survival rate inside its vector host—which may or may not affect vector fitness—and incubation or turnover rate that is inversely proportional to temperature[19]. Moreover, climate and human behavior changes increase human exposures to vectors and the pathogenic agents they transmit [20]. Studies of plague transmission in the U.S.A, China and Kazakhstan have found that the patterns of human or rodent plague are shifting as temperatures warms up or link to climatic oscillations (such as El Niño) and precipitation pattern [20].

Iranian physicians were familiar with the human plague for a long time. Although there are little information about the situation of plague from earlier centuries, more documented evidence are available from the 19th and 20th centuries. As a matter of fact, faunistic studies of Iranian fleas have been carried out mainly about 60 years ago in a context of plague research and most species described at the time were collected and described off plague hosts [21]. When plague research stopped, flea inventories did so too and there are no current updates on the flea fauna of Iran. However, a recent study detected antibodies against Y. pestis in dogs—known to be a good sentinels for plague surveillance- while human plague hasn’t been reported for 50 years [22]. This finding triggered some concern about the possible plague reemergence in the countryside, in the old plague foci and called for an update on the state-of-knowledge of the flea diversity in the country. The aims of the present study were to update by reviewing the current state of knowledge of the Iranian Siphonaptera diversity, their host range and especially the medically important species.

Methods

This review was based on a search of the online scientific databases (Scientific Information Database) PubMed and Google Scholar from 1952 through 31st August 2016. Keywords—submitted in English, French, Turkish and Russian—for the search were “flea AND fauna AND Iran”; “Iran AND puce”, “Iran AND siphonaptera”; “Iran AND ectoparasite”. Searches were conducted in the titles, abstracts, keywords and full text. The majority of our knowledge on the Siphonaptera of Iran is derived from plague studies[23], the concept of “telluric plague” is coeval with these researches[24] and studies of two flea specialists, the Iranian Farhang-Azad and the French J.M. Klein.

In each case the flea species, its host, and location of sampling were extracted from the published papers. The flea distribution maps were prepared using ArcGIS (ArcGIS version 9.3, ESRI). An online software were used to further classify and quantify the shared and exclusive vertebrate hosts of fleas with the “family or subfamily” filtering criteria[25].

Results

Literature review

The data for this study were extracted from about 100 relevant papers in English, French, Istanbul Turkish or Russian. Faunistic reviews of the medically significant fleas showed the presence of fleas through 31 Iranian provinces (Fig 1). In the old classification of Iran provinces used by Farhang-Azad (1972b), the Khorasan province, which was the largest province of Iran in the plague research era, is currently divided in three provinces namely Razavi Khorasan, North Khorasan, and South Khorasan. This means that the spatial scale of the flea range resolution is less accurate in the old literature as it covers a larger area where the flea and their host are not homogenously found. Based on the information in the studied papers, the sampling locations mainly were human houses, animal husbandry premises, poultry farms, and rodents’ burrows.

Fig 1

Distribution maps of studied fleas (sub-) family in Iran.

Flea diversity

According to the literature, about 117 species or subspecies of fleas belonging to 7 families and 35 genera have been described in Iran. Most flea species reported in the studied literature belonged to the Ceratophyllidae (n = 33), Leptopsyllidae (n = 24), Pulicidae (n = 21), Ctenophthalmidae (n = 20) and Coptopsyllidae (n = 9) families. The flea species of the Ischnopsyllidae (bat-fleas) and Vermipsyllidae (carnivore-fleas) families consisted of only 6 and 4 species of the whole collection respectively (Tables 1 and 2).

Table 1

Studied species, places of sampling and hosts of studied fleas.

Family	Subfamily	Fleas species	Associated host	Province (Locality)	Ref.
Ceratophyllidae	Ceratophyllinae	Callopsylla aff. Caspia	Lag: Ochotona rufescens	Razavi Khorasan (Mashhad)	[26]
		C. caspia caspia	Rod.: Microtus arvalis	Alborz Mountains	[27–28]
		C. saxatilis	Rod.: Microtus nivalis	East Azarbaijan (Tabriz)	[26–28]
		C. tiflovi	Rod.: Citellus fulvus; Lag.: Ochotona rufescens	Isfahan, Tehran (Daleh Tani), Semnan (Shahrood), South Khorasan (Tabas), Razavi Khorasan (Mashhad, Asi Bolagh Ghoochan), Golestan (Shahkooh)	[21, 26]
		Ceratophyllus fringillae	Birds: Motacilla alba, Galerida cristata, Passer domesticus	Isfahan (Oshtor-Jan, Ali Abad)	[26, 29]
		C. gallinae	Birds: Gallus gallus, Motacilla alba, Passer domesticus	Fars, Qazvin, Qom, Hormozgan, Isfahan (Ali Abad), Kerman, South Khorasan, Razavi Khorasan, Lorestan (Khorram-Abad), Kohgiluyeh and Boyer-Ahmad, Kurdistan, Tehran, Zanjan	[26, 29–30]
		C. spinosus	Carn.: Vulpes vulpes (acc., a bird’s flea)	Hamadan (Agh Bolagh Morshed)	[21, 26]
		Citellophilus trispinus	Rod.: Citellus fulvus	Tehran, Razavi Khorasan (Mashhad, Sabzevar, Asi Bolagh, Ghoochan, Lotf Abad, Akhlamad), South Khorasan (Tabas)	[21, 26]
		Myxopsylla jordani	Rod.: Dryomys nitedula	Razavi Khorasan (Mashhad)	[26–27]
		Nosopsyllus baltazardi	Rod.: Gerbillus nanus, G. cheesmani, Tatera indica, Meriones persicus, M. crassus, M. libycus, Rhombomys opimus	Tehran, Fars (Shiraz), Kerman	[26]
		N. consimilis	Rod.: Microtus socialis	Ardebil (Moghan)	[31]
		N. farahae	Rod.: Microtus socialis	West Azarbaijan (Urmia)	[31]
		N. fasciatus	Rod.: Rattus rattus, R. norvegicus, Mus musculus, Cricetulus migratorius, Nesokia indica, Allactaga williamsi, Mesocricetus auratus	Lorestan (Khorram-Abad, Weysian, Chaghalvand, Papi, Chegini, Zagheh), Tehran, Gilan (Rasht)	[21, 26, 32]
		N. fidus	Rod.: Gerbillus nanus	Sistan and Baluchestan (Zabol)	[31]
		N. iranus attenuates	Rod.: Meriones tristrami	Kurdistan	[27]
		N. iranus iranus	Rod.: Meriones persicus, M. libycus, M. vinogradovi, M. tristrami, Rattus norvegicus, Microtus irani, M. socialis, Cricetulus migratorius; Insect.: Hemiechinus auritus (acc.); Carn.: Vulpes vulpes (acc.)	Kurdistan, Tehran, Qazvin, Hamadan (Agh Bolagh Morshed, Akanlu), Lorestan (Khorram-Abad, Weysian, Chaghalvand, Papi, Chegeni, Zagheh), East Azarbaijan (Tabriz), West Azarbaijan (Urmia), Kermanshah, Ardebil (Bilesauvar)	[21, 26, 33–34]
		N. iranus theodori	NS	NS	[27]
		N. laeviceps gorganus	Rod.: Rhombomys opimus, Meriones libycus, M. persicus, Microtus socialis	Golestan (Dash Boroon)	[21, 26]
		N. londiniensis londiniensis	Rod.: Mus musculus	NS	[27]
		N. medus	Rod.: Mus musculus; Insect: Crocidura russula, C. leucodon	Kermanshah, Hamadan (Akanlu), West Azarbaijan (Urmia)	[21, 26, 35]
		N. mikulini (= N. parsus)	Rod.: Mus musculus, Rattus norvegicus, Cricetulus migratorius, Microtus irani, M. arvalis, M. socialis, Mesocricetus auratus, Meriones persicus, M. libycus, M. vinogradovi; Lag.: Ochotona rufescens, Lepus capensis; Carn.: Vulpes vulpes	Hamadan (Akanlu), Tehran (Daleh Tani), Kurdistan	[21, 26, 36]
		N. mokrzecki	Rod.: Cricetulus migratorius, Microtus socialis	East Azarbaijan (Tabriz)	[26]
		N. monstrosus vlasovi	Rod.: Rhombomys opimus	Razavi Khorasan (Lotf Abad)	[37]
		N. philipovi rashti	Rod.: Mus musculus, Calomyscus bailwardi, Ellobius fuscocapillus, Microtus arvalis, M. socialis	Tehran, Razavi Khorasan (Mashhad)	[26]
		N. pringlei	Rod.: Tatera indica, Rhombomys opimus, Jaculus jaculus, J. blanfordi, Meriones crassus, M. libycus, M. persicus, Gerbillus nanus	Isfahan (Yeklengy), Tehran (Seid Abad, Kan), Khuzestan (Shoosh). Markazi (Aziz Abad, Mahallat), Isfahan (Ghaleh Tappe)	[21, 26, 29]
		N. sarinus aryanus	Rod.: Rattus norvegicus	Khuzestan (Abadan)	[21, 26]
		N. sarinus parthius	Rod.: Mus musculus, Meriones persicus	Kerman, Fars (Shiraz)	[21, 26, 33]
		N. sarinus sarinus	Rod.: Mus musculus	NS	[27, 37]
		N. tersus tarsus	Rod.: Rhombomys opimus	NS	[26–27]
		N. turkmenicus turkmenicus	Rod.: Rhombomys opimus, Gerbillus nanus, Cricetulus migratorius, Meriones persicus, M. libycus	Razavi Khorasan (Sabzehvar, Ghoochan, Lotf Abad)	[26]
		N. vlasovi	Rod.: Rhombomys opimus, Meriones meridianus, M. crassus, M. libycus	Fars (Shiraz), Kerman	[26]
		N. ziarus	Rod.: Rhombomys opimus, Meriones persicus, M. libycus, Jaculus blanfordi	Isfahan	[21, 29]
		Paraceras melis melis	Carn.: Meles meles	Hamadan (Agh Bolagh Morshed, Akanlu, Ghare Dagh, Gueurach)	[21, 26]
Coptopsyllidae	NS	Coptopsylla bairamaliensis	Rod.: Rhombomys opimus, Meriones persicus	Razavi Khorasan (Hossain Abad, Loft Abad)	[26, 38–40]
		C. iranica	Rod.: Gerbillus nanus, Meriones libycus, M. persicus, M. meridianus, M. crassus	Golestan (Dash-Boroun), Isfahan, Razavi Khorasan (Lotf Abad), Tehran, Sistan and Baluchestan (Bampour, Zahedan), Yazd, South Khorasan (Tabas)	[38–39]
		C. joannae	NS	NS	[27]
		C. lamellifer dubinini	Rod.: Rhombomys opimus, Meriones vinogradovi, M. libycus, M. persicus; Carn.: Meles meles (acc.)	Golestan (DashBoroun), Razavi Khorasan (Loft Abad, Shandiz), Hamadan (Akanlu), Isfahan (Dorche Piaz, Yeklengy)	[21, 26, 29, 38–39]
		C. lamellifer lamellifer	Rod.: Rhombomys opimus, Meriones persicus, M. vinogradovi, M. libycus; Carn.: Meles meles (acc.).	Golestan (Torkman Sahra), Razavi Khorasan (Lotf Abad, Shandiz), Isfahan (Dorcheh)	[26, 38, 40]
		C. lamellifer rostrata	Rhombomys opimus	Chaharmahal and Bakhtiyari, Isfahan (Yeklengy, Dorche Piaz)	[26, 38, 41]
		C. mesghalii	Rhombomys opimus	Chaharmahal and Bakhtiyari, Isfahan (Yeklengy, Dorche Piaz)	[26, 29, 38–40]
		C. mofidii	Rod.: Tatera indica, Gerbillus nanus, Meriones libycus, M. crassus, M. persicus, Rhombomys opimus, Calomyscus bailwardi, Cricetulus migratorius	Fars (Fasa to Jahrom), Golestan (DashBoroun), Isfahan, Razavi Khorasan (Lotf Abad), Tehran, Kerman (Fahraj, Hossein Abad), Yazd (Taft), South Khorasan (Tabas)	[26, 38–39]
		C. neronovi	Rod.: Meriones persicus, M. crassus	Sistan and Baluchestan	[38]
Ctenophthalmidae	Anomiopsyllinae	Wagnerina schelkovnikovi	Rod.: Mus musculus, Calomyscus bailwardi, Cricetulus migratorius, Meriones persicus, Mesocricetus auratus, Nesokia indica	Tehran (Firooz Kooh, Ghale Morghi), Hamadan (Akanlu), West Azarbaijan (Urmia), Fars (Shiraz), Kerman	[21, 26]
	Ctenophthalminae	Ctenophthalmus angulosus	Insect: Crocidura russula; Rod.: Pitymys majori	Mazandaran (Veysar), Ghilan (Assalem)	[37]
		C. congener congener	Insect: Talpa europaea; Rod.: Apodemus sylvaticus, Meriones persicus, Microtus arvalis, M. socialis	NS	[42]
		C. congener nadimi	Rod.: Microtus arvalis	Razavi Khorasan (Mashhad)	[26–27, 43]
		C. dolichus bair	NS	Razavi Khorasan (Mashhad)	[26]
		C. dolichus kurdensis	Rod.: Cricetulus migratorius, Meriones persicus, M. libycus, M. vinogradovi	Kurdistan, Tehran	[21, 26, 44]
		C. iranus persicus	Rod.: Mesocricetus auratus, Cricetulus migratorius, Nesokia indica, Meriones persicus, M. libycus, M. vinogradovi, M. tristrami, Microtus irani, Mus musculus; Carn.: Vulpes vulpes (acc.)	Hamadan (Akanlu), Qazvin, East Azarbaijan (Tabriz)	[21, 26, 33]
		C. lewisi	Rod.: Pitymys majori	Mazandaran (Dasht-Lateh)	[37]
		C. proximus	Insect: Crocidura russula, C. leucodon; Rod.: Apodemus sylvaticus, A. mystacinus	Mazandaran (Veysar, Dasht-Lateh), Ghilan (Assalem), West Azarbaijan (Urmia)	[37]
		C. rettigi smiti	Rod.: Mesocricetus auratus, Allactaga williamsi	Hamadan (Agh Bolagh Morshed)	[21, 26, 36]
		Palaeopsylla copidophora	Insect: Talpa caeca	Ghilan (Assalem)	[37]
	Doratopsyllinae	Doratopsylla dampfi irana	Insect: Sorex minutus, Crocidura russula; Rod.: Apodemus mystacinus	Mazandaran (Veysar), Ghilan (Assalem)	[37]
	Neopsyllinae	Neopsylla pleskei ariana	Rod.: Citellus fulvus, Meriones persicus	Tehran (FiroozKooh), Razavi Khorasan (Mashhad)	[21, 26, 28, 45]
		N. setosa setosa	Rod.: Citellus fulvus, Cricetulus migratorius	Razavi Khorasan (Asi Bolagh Ghoochan)	[26]
		N. teratura rhagesa	Rod.: Cricetulus migratorius	Tehran, Kermanshah	[21, 26, 44]
	Rhadinopsyllinae	Rhadinopsylla bivirgis	Rod.: Meriones libycus, M. persicus	Razavi Khorasan (Asi Bolagh Ghoochan)	[26]
		R. syriaca	Rod.: Meriones libycus	Markazi (Aziz abad), Tehran, Kermanshah	[21, 26]
		R. ucrainica	Rod.: Meriones persicus, M. tristrami, M. libycus, M. vinogradovi, Mesocricetus auratus, Microtus irani,M. socialis, Cricetulus migratorius, Mus musculus	Tehran (Roodehen, Ghaleh Morghi, Seid Abad), Kurdistan, Hamadan (Agh Bolagh Morshed, Akanlu)	[21, 26]
	Stenoponiinae	Stenoponia tripectinata irakana (= S. insperata irakana)	Rod.: Gerbillus nanus, G. dasyurus, Meriones persicus, M. libycus, M. vinogradovi, M. tristrami, M. crassus, Calomyscus bailwardi, Tatera indica Rhombomys opimus, Citellus fulvus; Carn.: Meles meles	Khuzestan (Shoosh), Qazvin, Kurdistan, Hamadan (Akanlu) Tehran, East Azarbaijan (Tabriz), Kermanshah, Fars (Shiraz)	[21, 26, 34, 46]
		S. vlasovi	Rod.: Rhombomys opimus, Meriones persicus	Isfahan (Yeklengy), Razavi Khorasan (Mashhad)	[26, 29]
Ischnopsyllidae	Ischnopsyllinae	Chiropteropsylla brockmani	Chi.: Aselia tridens	Hormozgan (Roodan, Minab), Fars (Shiraz)	[26, 43]
		Ischnopsyllus dolosus	Chi.: Myotis blythi, Pipistrellus pipistrellus	Azarbaijan	[47]
		I. elongates	Chi.: Aselia tridens (acc.), Nyctalus noctula	Mazandaran (Tonekabon)	[47]
		I. octactenus	Chi.: Pipistrellus pipistrellus, Pipistrellus kuhlii	Ramsar, Ghilan (Rasht), Razavi Khorasan (Mashhad)	[21, 26, 37, 43, 48]
		I. petropolitanus	Chi.: Plecotus macrobullaris	Semnan (Gandab)	[47]
		Rhinolophopsylla unipectinata	Chi.: Rhinolophus blasii, Pipistrellus pipistrellus (acc.), Aselia tridens (acc.).	Razavi Khorasan (Mashhad)	[26, 47]
Leptopsyllidae	Amphipsyllinae	Amphipsylla argoi	Rod.: Calomyscus bailwardi	Isfahan (Ghaleh Tappeh)	[21, 26]
		A. parthiana	Rod.: Microtus socialis, M. arvalis	Razavi Khorasan (Mashhad)	[26–28]
		A. rossica rossica	Rod.: Microtus irani, М. Meles meles	Hamedan (Agh BolaghMorshed)	[21, 26]
		A. schelkovnikovi schelkovnikovi (= A. s. irana)	Rod.: Meriones persicus, M. libycus, M. vinogradovi, Mus musculus, Cricetulus migratorius, Rattus norvegicus, Microtus irani, Mesocricetus auratus; Carn.: Vulpes vulpes (acc.).	Hamadan (Agh Bolagh Morshed, Akanlu), Tehran (Firoozkooh), Isfahan (Ghaleh Tappeh), Razavi Khorasan (Mashhad)	[21, 26, 28]
		Ctenophyllus rufescens	Lag.: Ochotona rufescens; Rod.: Calomyscus bailwardi	Markazi (Mahallat)	[21, 26, 28]
		Frontopsylla ambigua	Rod.: Apodemus mystacinus, Mus musculus	Razavi Khorasan (Mashhad)	[26]
		Ophthalmopsylla volgensis arnoldi	Rod.: Allactaga elater, A. williamsi, Cricetulus migratorius, Meriones persicus, M. libycus, M. vinogradovi; Insect.: Hemiechinus auritus (acc.).	Hamadan (Agh Bolagh Morshed, Akanlu) Tehran, East Azarbaijan (Tabriz)	[21, 26]
		O. volgensis impersia	Rod.: Allactaga elater	Mazandaran (Sari)	[26, 49]
		O. volgensis intermedia	Rod.: Allactaga elater	Razavi Khorasan (Mashhad)	[26]
		Paradoxopsyllus grenieri	Rod.: Meriones persicus, M. vinogradovi	Hamadan (Akanlu)	[21, 26]
		P. microphthalmus	Rod.: Meriones persicus, Calomyscus bailwardi	Tehran (Firooz Kooh), Razavi Khorasan (Mashhad)	[21, 26, 28, 44]
		P. tikhomirovae	Rod.: Calomyscus bailwardi, Meriones persicus	Isfahan (Ghaleh Tappeh) Kerman, Fars (Shiraz), Razavi Khorasan (Mashhad)	[21, 26]
		Phaenopsylla tiflovi	Rod.: Calomyscus bailwardi	Isfahan (Ghaleh tappeh), Tehran, West Azarbaijan (Urmia)	[21, 26]
		P. kopetdag	Rod.: Calomyscus bailwardi	Tehran, Mazandaran (Sari), Kerman, Razavi Khorasan (Mashhad)	[26]
	Leptopsyllinae	Leptopsylla aethiopica aethiopica	Rod.: Mus musculus	Semnan	[50]
		L. putoraki	Insect: Crocidura leucodon	Tehran	[26]
		L. taschenbergi taschenbergi	Rod.: Apodemus mystacinus, A. sylvaticus, Rattus rattus, Mus musculus	Hamadan (Razan), Tehran, Gilan (Rasht), Mazandaran (Sari), East Azarbaijan (Tabriz), West Azarbaijan (Urmia), Kermanshah, Fars (Shiraz), Razavi Khorasan (Mashhad), Isfahan	[26, 51]
		L. segnis	Rod.: Rattus rattus, R. norvegicus, Mus musculus	Gilan (Rasht, Bandar Anzali), West Azarbaijan (Urmia), Kermanshah	[21, 26]
		Peromyscopsylla tikkoinirovae	Rod.: Calomyscus bailwardi	Isfahan (Ghaleh Tappe)	[20]
	Mesopsyllinae	Caenopsylla laptevi laptevi	Carn.: Vulpes vulpes, Rod.: Tatera indica	Isfahan (Shah-Lora, Mahyar), Fars (Shiraz, Kazerun), Markazi (Mahallat), Tehran (Hassan Abad), Kerman	[21, 26, 29, 52]
		Mesopsylla eucta tuschkan	Rod.: Allactaga elater, A. williamsi, Meriones vinogradovi, M. tristrami M. libycus, M. persicus, M. libycus, Cricetulus migratorius; Carn.: Vulpes vulpes (acc.)	Tehran (Kamal Abad), Hamadan (Agh Bolagh Morshed, Akanlu), Razavi Khorasan (Feiz Abad),	[21, 26]
		M. tuschkan mesa	Rod.: Allactaga williamsi, A. elater; Carn.: Vulpes vulpes	Razavi Khorasan (Mashhad)	[26–27]
		M. tuschkan tuschkan	Rod.: Allactaga williamsi, A. elater; Carn.: Vulpes vulpes	Tehran, Kermanshah	[26–27]
		M. eucta eucta	Rod.: Meriones libycus, M. persicus	Hamadan (Agh Bolagh Morshed, Akanlu), Razavi Khorasan (Feiz Abad), Tehran (Kamal Abad)	[21, 26]
Pulicidae	Archaeopsyllinae	Archaeopsylla erinacei erinacei	Insect.: Hemiechinus auritus	Isfahan (Goloon Abad), Hamadan (Agh Bolagh Morshed), Tehran (Youssef Abad),West Azarbaijan (Maku), East Azarbaijan (Maragheh, Marand)	[21, 26, 29, 37]
		Ctenocephalides canis	Carn.: Canis lupus familiaris, C. lupus pallipes, C. aureus, Vulpes vulpes, Meles meles, Mustela nivalis, Herpestes auropunctatus, Hyaena hyaena; Rod.: Tatera indica (acc.); Lag: Lepus europaeus (acc.).	Fars (Kazerun), Qazvin, Qom, Hormozgan, Isfahan, Ilam, Kerman, South Khorasan, Kohgilouyeh and Boyerahmad (Margoun, Loudab, Bakhsh-e Markazi), Razavi Khorasan, Lorestan (Khorram-Abad), Khuzestan (Ahvaz, Shoosh, Dezfool, Abadan), Tehran, Zanjan, Mazandaran (Tonekabon, Babolsar), Hamadan (Agh Bolagh Morshed)	[8, 21, 26, 29–30, 32, 53–56]
		C. felis felis	Carn.: Canis lupus familiaris, Felis catus, F. silvestris, C. lupus spp., Vulpes vulpes,V. rueppellii, Canis aureus, Mustela nivalis, Herpestes edwardsii, Hyaena hyaena; Rod.: Rattus norvegicus (acc. but not rare); Ungul.: Ovis aries, Capra hircus	West Azarbaijan, Ilam, Kurdistan, Kohgilouyeh and Boyerahmad (Margoun, Loudab, Bakhsh-e Markazi), Khuzestan (Shoosh, Abadan, Dezfool, Behbahan Ahvaz), Tehran, Golestan (Bandar Torkman), Isfahan, Gilan (Rasht), Fars (Kazerun), Razavi Khorasan (Mashhad)	[8, 21, 26, 32, 53, 57]
		C. orientis	Carn.: Canis lupus familiaris, C. lupus ssp., Vulpes vulpes, C. aureus, Felis catus; Rod.: Rattus rattus (acc. but not rare); Ungul.: Ovis aries, Capra hircus.	Hormozgan (Bandar Jask)	[26]
	Pulicinae	Echidnophaga gallinacean	Insect.: Hemiechinus auritus, Carn.: Meles meles (acc.).	Isfahan (Goloon Abad), Golestan (Bandar Torkman), Tehran (Youssef Abad), Qazvin	[21, 26, 29]
		E. oschanini	Rod.: Rhombomys opimus, Meriones persicus, M. libycus	Isfahan (Yeklengy, Ziar), Golestan (Dash Boroon)	[21, 26, 29]
		E. popovi	Carn.: Vulpes vulpes, Meles meles	Hamadan (Agh BolaghMorshed), Tehran (Hesarak), Qazvin	[21, 29]
		Parapulex chephrenis	Acomys sp.	NS	[27]
		Pulex irritans	Prim.: Homo sapiens; Carn.: Canis lupus familiaris, C. lupus pallipes, C. aureus, Vulpes vulpes, Meles meles, Herpestes auropunctatus, Pantera pardus, Hyaena hyaena; Ungul.: Ovis aries, Capra hircus, Bos taurus; Rod.: Rattusrattus (acc.); Insect.: Hemiechinus auritus, Artiodact.: Sus scrofa; Birds (acc.): Gallus gallus, Corvus corone	East Azarbaijan, Fars (Shiraz, Kazerun), Ghilan (Assalem), Golestan (Gorgan), Hamadan, Hormozgan, Isfahan (Yeklengi, Ziar, Varzaneh, Shahreza), Kerman, Kermanshah, Khuzestan (Abadan, Shoosh, Khoramshahr, Dezfool, Izeh, Soosangerd), Kohgilouyeh and Boyerahmad, Kurdistan, Lorestan (Khorram-Abad), Markazi, Mazandaran (Marzan Abad, Tonekabon), Persian Golf, Qazvin, Qom, Razavi Khorasan (Mashhad, Ghoochan), Semnan, South Khorasan, Tehran (Hesarak),West Azarbaijan (Miandoab), Zanjan,	[21, 29, 32, 35, 37, 54–55]
	Xenopsyllinae	Synosternus cleopatrae	Rod.: Tatera indica, Gerbillus nanus, G. cheesmani, Insect.: Hemiechinus megalotis	Sistan and Baluchestan (Chabahar, Zabol), Kerman	[26]
		S. pallidus	Rod.: Tatera indica; Insect.: Hemiechinus auritus, H. megalotis; Carn.:Vulpes vulpes, V. rueppellii, Canis lupus, Herpestes auropunctatus, Hyaena hyaena	Khuzestan (Dezfool, Abadan, Shoosh) Bushehr (Borazjan), Tehran (Kamal Abad, Hesarak), Markazi (Mahallat)	[21, 26]
		Xenopsylla astia	Rod.: Rattus norvegicus, R. rattus,Tatera indica, Calomyscus bailwardi, Meriones crassus, M. hurrianae, Citellus fulvus, Nesokia indica, Jaculus jaculus, Mus musculus, Acomys dimidiatus; Insect.: Hemiechinus auritus	Kohgilouyeh and Boyer Ahmad, Kurdistan, Khuzestan (Abadan, Dezfool, Soosangerd, Shoosh), Hormozgan (Bandare Abbas), Kermanshah (Ghasre Shirin), Fars (Kazerun), Razavi Khorasan (Mashhad), Isfahan (Ghale Tappe)	[21, 26, 28, 32, 58–59]
		X. buxtoni	Rod.: Rattus norvegicus, R. rattus, Mus musculus, Tatera indica, Meriones persicus, M. tristrami, M. libycus, M. vinogradovi, Microtus arvalis, M. irani, M. socialis, Nesokia indica, Cricetulus migratorius, Mesocricetus auratus, Allactaga elater, A. williamsi; Carn.:Vulpes vulpes (acc.), Meles meles	Kurdistan, Hormozgan, Lorestan (Khorram-Abad, Weysian, Chaghalvand, Papi, Chegeni, Zagheh), Kermanshah (Sarpole Zahab), Kohgilouyeh and Boyerahmad (Margoun, Loudab, Bakhsh-e Markazi), Tehran (Roudehen Morabad, Ghale Morghi, Talow, Vanak), Qazvin, Markazi (Mahallat), Hamadan (Malayer, Agh Bolagh Morshed, Akanlu), Fars (Kazerun), Qazvin	[21, 26, 32, 34–35, 57–58, 60]
		X. cheopis cheopis	Rod.: Rattus norvegicus, R. rattus, Mus musculus, Citellus fulvus, Cricetulus migratorius, Meriones persicus	Hormozgan (Bandar abbas), Khuzestan (Ahvaz, Shoosh), Gilan (Rasht, Bandar anzali), Golestan (Bandar torkman), Tehran, Isfahan, Razavi Khorasan (Darreh gaz), South Khorasan (Tabas)	[8, 21, 26, 54, 59]
		X. conformis conformis	Rod.: Allactaga elator, Tatera indica, Rhombomys opimus, Jaculus jaculus, J. blanfordi, Gerbillus nanus, Meriones tristrami, M. crassus, M. persicus, M. vinogradovi, M. tristrami, M. meridianus, M. libycus, Citellus fulvus, Cricetulus migratorius, Nesokia indica, Calomyscus bailwardi; Insect.: Hemiechinus megalotis	Sistan and Baluchestan (Daman, Qasre Qand, Bampour), Kurdistan, Isfahan (Yeklengy, Ghaleh tappeh), Tehran (Hassan Abad, Kan, Najm Abad, Kamal Abad, Hesarak, Seid Abad), Razavi Khorasan (Mashhad, Mosen Abad, Feiz Abad, Darreh Gaz, Sange Atesh), Khuzastan (Shoosh), South Khorasan (Tabas), Kermanshah (Shahmar), Golestan (Dash Boroon), Qazvin, Markazi (Aziz Abad)	[21, 26, 28–29, 32, 58]
		X. conformis mycerini	Rod.: Allactaga elator	Razavi Khorasan (Mashhad)	[28, 44]
		X. gerbilli gerbilli	Rod.: Rhombomys opimus	Razavi Khorasan (Darreh Gaz, Lotf Abad)	[26]
		X. hussaini	Rod.: Nesokia indica, Tatera indica, Gerbillus nanus, G. cheesmani, Meriones persicus, Insect.: Hemiechinus megalotis	Fars (Shiraz), Kerman	[26]
		X. nubica	Rod.: Allactaga elator, Jaculus jaculus, J. blanfordi	Sistan and Baluchestan (Daman, Qasre Qand, Bampour), Isfahan (Harrand)	[26, 28–29, 58]
		X. nuttalli	Rod.: Rhombomys opimus, Gerbillus nanus,G. cheesmani, Meriones persicus, M. crassus, M. meridianus, Nesokia indica, Hystrix indica, Mus musculus, Calomyscus bailwardi, Tatera indica, Ellobius fuscocapillus; Insect.: Hemiechinus auritus; Carn.: Vulpes vulpes; Ungul.: Ovis aries, Bos taurus, Capra hircus; Lag.: Lepus capensis, Ochotona rufescens, Chi.: Pipistrellus pipistrellus (acc.)	Kohgilouyeh and Boyerahmad (Bakhsh-e Markazi, Margoun, Loudab), Isfahan (Shahreza), Golestan (Dash Boroon), Razavi Khorasan (Sabzehevar)	[21, 26, 29, 32, 61]
		X. persica	Rod.: Meriones persicus, Rhombomys opimus	Razavi Khorasan (Asi Bolagh Ghoochan)	[5, 26]
Vermipsyllidae	NS	Chaetopsylla globiceps	Carn.: Vulpes vulpes	Isfahan (Shah-Lora, Khansar, Shahreza) Mashhad, Fars (Shiraz)	[21, 26, 29]
		C. hyaenae	Carn.: Hyaena hyaena	Tehran	[21, 26]
		C. korobkovi	Carn.: Vulpes vulpes	Hamadan (Agh Bolagh Morshed, Akanlu) Isfahan (Shahreza, Shah-Lora), Fars (Shiraz)	[21, 26, 29]
		C. trichosa avicenni (= C. trichosa)	Carn.: Meles meles	Kurdistan	[21, 44]

Abbreviations: Carn.: Carnivora, Rod.: Rodentia, Lag.: Lagomorpha, Insect.: Insectivora, Ungul.: Ungulate, Prim.: Primates, Chi.: Chiroptera, Artiodact.: Artiodactyla, acc.: accidental host. NS: Not Stated. * In the old classification of Iran provinces which implied by Farhang-Aazad (1972b)[62], the main cities were regarded as flea collection locality [26].

Table 2

Comparison of taxonomic data on Siphonaptera and their host orders represented in Iran with the counterpart ones in the world [5, 63].

Family	Distribution (region)	Subfamily		Genera		Species / Subspecies		Major host
		World	Iran	World	Iran	World	Iran	World	Iran
Ceratophyllidae	Cosmopolitan but predominantly Holarctic	2	1	44	6	403	33	Primarily rodents, occasionally viverrids, mustelids, birds, and a single species on an insectivore (Siberian mole)	Rodentia (71.05%) Birds (10.53%), Insectivora (7.89%), Carnivora (5.26%) and Lagomorpha (5.26%)
Coptopsyllidae	Palearctic	0	0	1	1	19	9	Rodents (gerbils and their allies)	Rodentia (90.91%) and Carnivora (9.09%)
Ctenophthalmidae	Primarily Holarctic, and Afrotropical some in southern hemisphere	9	6	42	7	548	20	Rodents, occasionally pikas, insectivores (shrews and moles), marsupials, and a single species on mustelids	Rodentia (75.86%), Insectivora (17.24%) and Carnivora (6.9%)
Ischnopsyllidae	Cosmopolitan	2	1	20	3	122	6	Chiroptera	Chiroptera (100%)
Leptopsyllidae	Palearctic, Nearctic, Oriental, a few species in Australian or Ethiopian regions	*2	*3	29	10	230	24	Rodents, lagomorphs (hares, rabbits, pikas), insectivores, and rarely elephant shrews and foxes	Rodentia (80.95%), Insectivora (9.52%), Lagomorpha (4.76%) Carnivora (4.76%)
Pulicidae (includes erroneously tungid flea)	Cosmopolitan	6	3	27	7	182	21	Very broad host range, including carnivores, ungulates, bats, edentales (armadillos), and occasionally birds (Cariama spp).	Rodentia (52.63%), Ungulates (5.26%), Carnivora (24.56%), Artiodactyla (1.75%), Insectivora (3.51%), Birds (3.51%), Chiroptera (1.75%), Primates (1.75%) and Lagomorpha (5.26%)
Vermipsyllidae	Holarctic	0	0	3	1	39	4	Carnivores and ungulates	Carnivora (100%)
Total		21	14	166	35	1543	117

* Altough Leptopsyllidae further classified as subfamilies Amphipsyllinae and Leptopsyllinae and the tribes Amphipsyllini and Leptopsyllini [64] but Klein (1963) was regarded Mesopsyllinae as third subfamily in the Leptopsyllidae of Iran [21].

The Ceratophyllidae, the more represented flea family, consisted of 33 species belonging to 6 genera, comprising Callopsylla, Ceratophyllus, Citellophilus, Myoxopsylla, Nosopsyllus and Paraceras.

The Leptopsyllidae, bird and rodent fleas, consisted of 24 species consisting of 10 genera including Amphipsylla, Caenopsylla, Ctenophyllus, Frontopsylla, Leptopsylla, Mesopsylla, Ophthalmopsylla, Paradoxopsyllus, Peromyscopsylla and Phaenopsylla.

The Ctenophthalmidae consisted of 20 species belonging to 7 genera comprising Ctenophthalmus, Doratopsylla, Neopsylla, Palaeopsylla, Rhadinopsylla, Stenoponia and Wagnerina.

The Pulicidae, a cosmopolitan family of the most notorious plague vectors (genus Xenopsylla), included 21 species distributed in 7 genera comprising Archaeopsylla, Ctenocephalides, Echidnophaga, Pulex, Synosternus, Parapulex, and Xenopsylla.

The Coptopsyllidae was limited to 9 species in the genus Coptopsylla.

In the above-mentioned five families, the most commonly reported fleas belong to the genera Nosopsyllus (Ceratophyllinae), Xenopsylla (Xenopsyllinae), Ctenophthalmus (Ctenophthalminae) Coptopsylla (Coptopsyllidae) Amphipsylla (Amphipsyllinae), Leptopsylla (Leptopsyllinae), and Mesopsylla (Mesopsyllinae). Detailed information is presented in Table 1.

Host diversity and associated flea fauna

The hosts associated with Iran fleas ranged from the small mammals (Rodentia, Chiroptera, Lagomorpha, Insectivora) to the large mammals (Ungulata, Carnivora, Primates, Artiodactyla) and birds as well. On the whole, 166 vertebrate host species were reported infested by fleas in Iran in the literature including Pulicidae (n = 56), Ceratophyllidae (n = 38), Ctenophthalmidae (n = 29), Leptopsyllidae (n = 22), Coptopsyllidae (n = 11), Ischnopsyllidae (n = 7) and Vermipsyllidae (n = 3). By filtering the compiled data, we recognized 77 vertebrate host species among all seven flea families.

Eight potential mammals were hosted by ≤7 flea (sub-) family respectively; these were: Calomyscus bailwardi (7), Meles meles (7), Mus musculus (7), Meriones vinogradovi (8), Vulpes vulpes (8), Cricetulus migratorius (9), Meriones libycus (9) and Meriones persicus (11). Actually flea (sub-) families can infest ≥10 vertebrate hosts were Xenopsyllinae (n = 43), Ceratophyllinae (n = 37), Archaeopsyllinae (n = 20), Ctenophthalminae (n = 20), Pulicinae (n = 19), Amphipsyllinae (n = 17), Stenoponiinae (n = 12) and Coptopsyllidae (n = 11). Detailed information is presented in Table 3.

Table 3

Common mammal hosts in Iran and their flea diversity at the family and subfamily levels.

Host	Typical habitat	(sub-) family															Total flea (sub-) families per host
		Ce	Co	An	Ct	Do	Ne	Rh	St	Am	Le	Me	Ar	Pu	Xe	Ve
Acomys dimidiatus	semi-arid or dry habitats	-	-	-	-	-	-	-	-	-	-	-	-	-	1	-	1
Allactaga elater	deserts and semideserts	-	-	-	-	-	-	-	-	1	-	1	-	-	1	-	3
Allactaga williamsi	steppe regions with sparse vegetation	1	-	-	1	-	-	-	-	1	-	1	-	-	1	-	5
Apodemus mystacinus	forest with rocky areas	-	-	-	1	1	-	-	-	1	1	-	-	-	-	-	4
Apodemus sylvaticus	wide variety of semi-natural habitats	-	-	-	1	-	-	-	-	-	1	-	-	-	-	-	2
Bos Taurus	rangelands	-	-	-	-	-	-	-	-	-	-	-	-	1	1	-	2
Calomyscus bailwardi	barren, dry and rocky mountainsides	1	1	1	-	-	-	-	1	1	1	-	-	-	1	-	7
Canis aureus	dry habitats	-	-	-	-	-	-	-	-	-	-	-	1	1	-	-	2
Canis lupus spp.	arid desert regions to dense scrub forests	-	-	-	-	-	-	-	-	-	-	-	1	-	1	-	2
Canis lupus familiaris	northern habitats with sufficient prey	-	-	-	-	-	-	-	-	-	-	-	1	1	-	-	2
Canis lupus pallipes	northern habitats with sufficient prey	-	-	-	-	-	-	-	-	-	-	-	1	1	-	-	2
Capra hircus	rangelands	-	-	-	-	-	-	-	-	-	-	-	1	1	1	-	3
Citellus fulvus	deserts and semi-deserts	1	-	-	-	-	1	-	1	-	-	-	-	-	1	-	4
Cricetulus migratorius	arid or semi-arid regions	1	1	1	1	-	1	1	-	1	-	1	-	-	1	-	9
Crocidura leucodon	moist mountainous regions	1	-	-	1	-	-	-	-	-	1	-	-	-	-	-	3
Crocidura suaveolens	arid areas with moist vegetation	1	-	-	1	1	-	-	-	-	-	-	-	-	-	-	3
Dryomys nitedula	broad variety of woodlands	1	-	-	-	-	-	-	-	-	-	-	-	-	-	-	1
Ellobius fuscocapillus	open steppes habitat with loose soil	1	-	-	-	-	-	-	-	-	-	-	-	-	1	-	2
Felis catus	cosmopolitan domestic species	-	-	-	-	-	-	-	-	-	-	-	1	-	-	-	1
Felis silvestris	areas with rocks and tall trees	-	-	-	-	-	-	-	-	-	-	-	1	-	-	-	1
Gerbillus cheesmani	sandy soils and mud flats	1	-	-	-	-	-	-	-	-	-	-	-	-	1	-	2
Gerbillus dasyurus	desert, semi-desert, and rocky habitats	-	-	-	-	-	-	-	1	-	-	-	-	-	-	-	1
Gerbillus nanus	desert, semi-desert, arable land and gardens	1	1	-	-	-	-	-	1	-	-	-	-	-	1	-	4
Hemiechinus auritus	dry steppes, semi-deserts and deserts	1	-	-	-	-	-	-	-	1	-	-	1	1	1	-	5
Hemiechinus megalotis	mountainous areas	-	-	-	-	-	-	-	-	-	-	-	-	-	1	-	1
Herpestes auropunctatus	scrublands and dry forest	-	-	-	-	-	-	-	-	-	-	-	1	1	1	-	3
Herpestes edwardsii	thickets, cultivated fields or broken, bushy vegetation	-	-	-	-	-	-	-	-	-	-	-	1	-	-	-	1
Homo sapiens	passim	-	-	-	-	-	-	-	-	-	-	-	-	1	-	-	1
Hyaena hyaena	arid to semi-arid environments	-	-	-	-	-	-	-	-	-	-	-	1	1	1	1	4
Hystrix indica	broad range of habitats	-	-	-	-	-	-	-	-	-	-	-	-	-	1	-	1
Jaculus blanfordi	desert with clay soil	1	-	-	-	-	-	-	-	-	-	-	-	-	1	-	2
Jaculus Jaculus	sandy or rocky deserts	1	-	-	-	-	-	-	-	-	-	-	-	-	1	-	2
Lepus capensis	Shrubs to open habitats	1	-	-	-	-	-	-	-	-	-	-	-	-	1	-	2
Lepus europaeus	open fields and pastures	-	-	-	-	-	-	-	-	-	-	-	1	-	-	-	1
Meles meles	woodlands	1	1	-	-	-	-	-	1	-	-	-	1	1	1	1	7
Meriones crassus	dry habitats in sandy deserts	1	1	-	-	-	-	-	1	-	-	-	-	-	1	-	4
Meriones hurrianae	sandy plains with higher density of bushes	-	-	-	-	-	-	-	-	-	-	-	-	-	1	-	1
Meriones libycus	arid or semi-arid regions	1	1	-	1	-	-	1	1	1	-	1	-	1	1	-	9
Meriones meridianus	sand deserts	1	1	-	-	-	-	-	-	-	-	-	-	-	1	-	3
Meriones persicus	arid, rocky, mountainous region	1	1	1	1	-	1	1	1	1	-	1	-	1	1	-	11
Meriones tristrami	steppe and semi-desert habitats	1	-	-	1	-	-	1	1	-	-	1	-	-	1	-	6
Meriones vinogradovi	semi desert, bare mountains and wastelands	1	1	-	1	-	-	1	1	1	-	1	-	-	1	-	8
Mesocricetus auratus	arable fields with annual crops	1	-	1	1	-	-	1	-	1	-	-	-	-	1	-	6
Microtus arvalis	moist meadows, moist and forest steppe, agricultural areas	1	-	-	1	-	-	-	-	1	-	-	-	-	1	-	4
Microtus irani	mountainous ranges	1	-	-	1	-	-	1	-	1	-	-	-	-	1	-	5
Microtus nivalis	mountainous ranges	1	-	-	-	-	-	-	-	-	-	-	-	-	-	-	1
Microtus socialis	steppe habitats	1	-	-	1	-	-	1	-	1		-	-	-	1	-	5
Mus musculus	cosmopolitan domestic species	1	-	1	1	-	-	1	-	1	1	-	-	-	1	-	7
Mustela nivalis	wide range of habitats	-	-	-	-	-	-	-	-	-	-	-	1	-	-	-	1
Nesokia indica	dry deciduous forests, scrublands, grasslands, arable land, pastures, plantations	1	-	1	1	-	-	-	-	-	-	-	-	-	1	-	4
Ochotona rufescens	mountainous regions	1	-	-	-	-	-	-	-	1	-	-	-	-	1	-	3
Ovis aries	cosmopolitan domestic species	-	-	-	-	-	-	-	-	-	-	-	1	1	1	-	3
Pantera pardus	wide range of habitats	-	-	-	-	-	-	-	-	-	-	-	-	1	-	-	1
Pipistrellus pipistrellus	wide range of habitats (Gorgan city, Golestan Province)	-	-	-	-	-	-	-	-	-	-	-	-	-	1	-	1
Pitymys majori	mixed forests	-	-	-	1	-	-	-	-	-	-	-	-	-	-	-	1
Rattus norvegicus	lowland and coastal regions	1	-	-	-	-	-	-	-	1	1	-	1	-	1	-	5
Rattus rattus	natural and semi-natural habitats	1	-	-	-	-	-	-	-	-	1	—	1	1	1	-	5
Rhombomys opimus	desert to semi-desert habitats	1	1	-	-	-	-	-	1	-	-	-	-	1	1	-	5
Sorex minutes	wide variety of habitats	-	-	-	-	1	-	-	-	-	-	-	-	-	-	-	1
Sus scrofa	a wide variety of temperate and tropical habitats	-	-	-	-	-	-	-	-	-	-	-	-	1	-	-	1
Talpa caeca	deciduous woodland, meadows and pastures in hilly or mountainous areas	-	-	-	1	-	-	-	-	-	-	-	-	-	-	-	1
Talpa europaea	deep soils	-	-	-	1	-	-	-	-	-	-	-	-	-	-	-	1
Tatera indica	arid habitats	1	1	-	-	-	-	-	1	-	-	1	1	-	1	-	6
Vulpes rueppellii	sand and stony deserts	-	-	-	-	-	-	-	-	-	-		1	-	1	-	2
Vulpes vulpes	tundra, desert and forest, as well as in city centres	1	-	-	1	-	-	-	-	1	-	1	1	1	1	1	8
Total host/flea (sub-) families		37	11	6	20	3	3	9	12	17	7	9	20	19	43	3	215 219

Ce Ceratophyllinae, Co Coptopsyllidae, An Anomiopsyllinae, Ct Ctenophthalminae, Do Doratopsyllinae, Ne Neopsyllinae, Rh Rhadinopsyllinae, St Stenoponiinae, Am Amphipsyllinae, Le Leptopsyllinae, Me Mesopsyllinae, Ar Archaeopsyllinae, Pu Pulicinae, Xe Xenopsyllinae and Ve Vermipsyllidae

At least 23, 6, 5, 5 and 1 host species are exclusively infested by Pulicidae, Ischnopsyllidae, Ceratophyllidae, Ctenophthalmidae and Leptopsyllidae respectively. However restricted host species was not found in the Coptopsyllidae and Vermipsyllidae (Table 4).

Table 4

Shared and exclusive vertebrate species associated with seven flea families of Pulicidae, Ceratophyllidae, Ctenophthalmidae, Leptospyllidae, Coptopsyllidae, Ischnopsyllidae and Vermipsyllidae in Iran.

Flea family(s)	No of host(s)	Vertebrate host(s)
Ceratophyllidae, Coptopsyllidae, Ctenophthalmidae, Leptopsyllidae and Pulicidae	6	Calomyscus bailwardi, Cricetulus migratorius, Meriones libycus, Meriones persicus, Meriones vinogradovi and Tatera indica
Ceratophyllidae, Coptopsyllidae, Ctenophthalmidae, Pulicidae and Vermipsyllidae	1	Meles meles
Ceratophyllidae, Ctenophthalmidae, Leptopsyllidae, Pulicidae and Vermipsyllidae	1	Vulpes vulpes
Ceratophyllidae, Coptopsyllidae, Ctenophthalmidae and Pulicidae	3	Gerbillus nanus, Meriones crassus and Rhombomys opimus
Ceratophyllidae, Ctenophthalmidae, Leptopsyllidae and Pulicidae	7	Allactaga williamsi, Meriones tristrami, Mesocricetus auratus, Microtus arvalis, Microtus irani, Microtus socialis and Mus musculus
Ceratophyllidae, Coptopsyllidae and Pulicidae	1	Meriones meridianus
Ceratophyllidae, Ctenophthalmidae and Leptopsyllidae	1	Crocidura leucodon
Ceratophyllidae, Ctenophthalmidae and Pulicidae	2	Citellus fulvus, Nesokia indica
Ceratophyllidae, Leptopsyllidae and Pulicidae	4	Hemiechinus auritus, Ochotona rufescens, Rattus norvegicus and Rattus rattus
Ceratophyllidae and Ctenophthalmidae	1	Crocidura russula
Ceratophyllidae and Pulicidae	6	Ellobius fuscocapillus, Gallus gallus, Gerbillus cheesmani, Jaculus blanfordi, Jaculus jaculus and Lepus capensis
Ctenophthalmidae and Leptopsyllidae	2	Apodemus mystacinus and Apodemus sylvaticus
Ischnopsyllidae and Pulicidae	1	Pipistrellus pipistrellus
Pulicidae and Vermipsyllidae	1	Hyaena hyaena
Ceratophyllidae	5	Dryomys nitedula, Galerida cristata, Microtus nivalis, Motacilla alba and Passer domesticus
Ctenophthalmidae	5	Gerbillus dasyurus, Pitymys majori, Sorex minutes, Talpa caeca and Talpa europaea
Ischnopsyllidae	6	Aselia tridens, Myotis blythi, Nyctalus noctula, Pipistrellus kuhlii, Plecotus macrobullaris and Rhinolophus blasii
Leptopsyllidae	1	Allactaga elater
Pulicidae	23	Acomys dimidiatus, Allactaga elator, Bos taurus, Canis aureus, Canis lupus familiaris, Canis lupus pallipes, Canis lupus spp., Capra hircus, Corvus corone, Felis catus, Felis silvestris, Hemiechinus megalotis, Herpestes auropunctatus, Herpestes edwardsi, Homo sapiens, Hystrix indica, Lepus europaeus, Meriones hurrianae, Mustela nivalis, Ovis aries, Pantera pardus, Sus scrofa and Vulpes ruppelli

A total of 53 vertebrate species were reported infested by six subfamilies of Ctenophthalmidae including Ctenophthalminae (n = 20), Stenoponiinae (n = 12), Rhadinopsyllinae (n = 9), Anomiopsyllinae (n = 6), Doratopsyllinae (n = 3) and Neopsyllinae (n = 3). By filtering the compiled data, 29 vertebrate host species were distinguished among all six subfamilies. Correspondingly 8, 6 and 1 host species are exclusively included in the Ctenophthalminae, Stenoponiinae and Doratopsyllinae. However there were not found any restricted vertebrate host species in the Anomiopsyllinae, Neopsyllinae and Rhadinopsyllinae (Table 5).

Table 5

Shared and exclusive vertebrate species associated with six subfamilies of Ctenophthalmidae in Iran.

Flea sub family(s)	No of host (s)	Vertebrate host(s)
Anomiopsyllinae, Ctenophthalminae, Neopsyllinae, Rhadinopsyllinae and Stenoponiinae	1	Meriones persicus
Anomiopsyllinae, Ctenophthalminae, Neopsyllinae and Rhadinopsyllinae	1	Cricetulus migratorius
Anomiopsyllinae, Ctenophthalminae and Rhadinopsyllinae	2	Mesocricetus auratus and Mus musculus
Ctenophthalminae, Rhadinopsyllinae and Stenoponiinae	3	Meriones libycus, Meriones tristrami and Meriones vinogradovi
Anomiopsyllinae and Ctenophthalminae	1	Nesokia indica
Anomiopsyllinae and Stenoponiinae	1	Calomyscus bailwardi
Ctenophthalminae and Doratopsyllinae	2	Apodemus mystacinus and Crocidura russula
Ctenophthalminae and Rhadinopsyllinae	2	Microtus irani and Microtus socialis
Neopsyllinae and Stenoponiinae	1	Citellus fulvus
Ctenophthalminae	8	Allactaga williamsi, Apodemus sylvaticus, Crocidura leucodon, Microtus arvalis, Pitymys majori, Talpa caeca, Talpa europaea and Vulpes vulpes
Doratopsyllinae	1	Sorex minutes
Stenoponiinae	6	Gerbillus dasyurus, Gerbillus nanus, Meles meles, Meriones crassus, Rhombomys opimus and Tatera indica

A total of 33 vertebrate species were reported infested by three subfamilies of Leptopsyllidae including Amphipsyllinae (n = 17), Mesopsyllinae (n = 9) and Leptopsyllinae (n = 7). By filtering the compiled data, 22 vertebrate host species were distinguished among three subfamilies. Investigation on the flea-host associations in subfamilies of the Leptopsyllidae showed that there were no common host species shared by the three subfamilies. However 6, 3 and 2 host species are exclusively included in the Amphipsyllinae, Leptopsyllinae and Mesopsyllinae respectively (Table 6).

Table 6

Shared and exclusive vertebrate species associated with three subfamilies of Ctenophthalmidae in Iran.

Flea sub family(s)	No of host (s)	Vertebrate host(s)
Amphipsyllinae and Leptopsyllinae	4	Apodemus mystacinus, Calomyscus bailwardi, Mus musculus and Rattus norvegicus
Amphipsyllinae and Mesopsyllinae	7	Allactaga elater, Allactaga williamsi, Cricetulus migratorius, Meriones libycus, Meriones persicus, Meriones vinogradovi and Vulpes vulpes
Amphipsyllinae	6	Hemiechinus auritus, Mesocricetus auratus, Microtus arvalis, Microtus irani, Microtus socialis and Ochotona rufescens
Leptopsyllinae	3	Apodemus sylvaticus, Crocidura leucodon and Rattus rattus
Mesopsyllinae	2	Meriones tristrami and Tatera indica

A total of 83 vertebrate species were reported infested by three subfamilies of Pulicidae including Xenopsyllinae (n = 43), Pulicinae (n = 20) and Archaeopsyllinae (n = 20). By filtering the compiled data, 56 vertebrate host species were distinguished among three subfamilies. Exploration of flea-host associations in Pulicidae pointed out that there are eight common hosts including Capra hircus (Linnaeus, 1758), Hemiechinus auritus (Gmelin, 1770), Herpestes auropunctatus (Hodgson, 1836), Hyaena hyaena (Linnaeus, 1758), Meles meles (Linnaeus, 1758), Ovis aries (Linnaeus, 1758), Rattus rattus (Linnaeus, 1758) and Vulpes vulpes (Linnaeus, 1758) among three subfamilies. Although a number of 27, 5 and 5 host species are exclusively included in the Xenopsyllinae, Pulicinae and Archaeopsyllinae respectively (Table 7).

Table 7

Shared and exclusive vertebrate species associated with three subfamilies of Pulicidae in Iran.

Flea sub family(s)	No of host (s)	Vertebrate host(s)
Archaeopsyllinae, Pulicinae and Xenopsyllinae	8	Capra hircus, Hemiechinus auritus, Herpestes auropunctatus, Hyaena hyaena, Meles meles, Ovis aries, Rattus rattus and Vulpes vulpes
Archaeopsyllinae and Pulicinae	3	Canis aureus, Canis lupus familiaris and Canis lupus pallipes
Archaeopsyllinae and Xenopsyllinae	4	Canis lupus spp., Rattus norvegicus, Tatera indica and Vulpes ruppelli
Pulicinae and Xenopsyllinae	4	Bos Taurus, Meriones libycus, Meriones persicus and Rhombomys opimus
Archaeopsyllinae	5	Felis catus, Felis silvestris, Herpestes edwardsi, Lepus europaeus and Mustela nivalis
Pulicinae	5	Corvus corone, Gallus gallus, Homo sapiens, Pantera pardus and Sus scrofa
Xenopsyllinae	27	Gerbillus cheesmani, Hystrix indica, Allactaga williamsi, Calomyscus bailwardi, Microtus irani, Cricetulus migratorius, Microtus arvalis, Jaculus jaculus, Ochotona rufescens, Gerbillus nanus, Pipistrellus pipistrellus, Nesokia indica, Meriones vinogradovi, Mesocricetus auratus, Mus musculus, Meriones crassus, Allactaga elater, Ellobius fuscocapillus, Acomys dimidiatus, Hemiechinus megalotis, Meriones tristrami, Citellus fulvus, Meriones hurrianae, Microtus socialis, Jaculus blanfordi, Lepus capensis, and Meriones meridianus

Discussion

The literature inventory of the fleas of Iran showed that there are seven Siphonaptera families in this country namely Ceratophyllidae, Leptopsyllidae, Pulicidae, Ctenophthalmidae, Coptopsyllidae, Ischnopsyllidae and Vermipsyllidae. These flea families are distributed in all parts of the country where sampling occurred and where data were available. According to the literature reviewed, the distribution range of those families extends in Hamadan and Kurdistan (West Iran) provinces rather than in Ardabil (northwest), Northern Khorasan (northeast), Bushehr (south), Mazandaran, Golestan and Gilan provinces (north). This fact is partly due to a collection bias in plague foci during the sixties (1963–1975 Baltazard, Klein, Farhang-Azad and Mollaret)[65-70]. The distribution maps of the studied fleas showed that further sampling, especially from provinces with poor faunistical studies, is necessary, especially in a context of vector-borne disease epidemiology where known mammalian hosts of pathogenic agents are also present.

Most fleas of medical or veterinary importance belong to the Ceratophyllidae, Leptopsyllidae, Pulicidae, Ctenophthalmidae and Vermipsyllidae families [12]. Pulicidae, a family including most cosmopolitan flea species of medical importance and in particular the Xenopsylla genus, was by far the most reported family in Iran [8, 29–30, 32, 35, 53–55, 57–60]. Analysis of common mammal hosts and their flea diversity revealed that M. persicus was infested by 11 flea subfamilies and Xenopsyllinae were hosted by at least 43 mammal species.

The Persian Jird, M. persicus, is distributed from Eastern Anatolia to Afghanistan and western Pakistan. Iran is the most extensive geographical region in the distribution range of the Persian Jird; indeed five of the six subspecies are found in the country [71].

At the first, the research team of Baltazard (1952) and then Golvan & Rioux (1963) and Poland and Dennis (1999) offered initial illustrations of the role of resistant or silent enzootic reservoirs in the maintenance of Y. pestis and human plague outbreaks in the Kurdistan focus. They showed that M. vinogradovi and M. tristrami were extremely sensitive to Y. pestis while M. libycus and M. persicus were highly resistant. Tatera indica has also been associated with transmission of Y. pestis in the country. Flea densities were reported to be high on M. persicus [23, 72–73]. In that era flea species including Pulex irritans, Xenopsylla cheopis, X. astia, X. buxtoni, X. conformis, Nosopsyllus fasciatus N. iranus iranus, and Stenoponia tripectinata were listed as favorite candidate Y. pestis vectors within and among vertebrates including man [74-79].

In 1980, Karimi et al. surveyed the Sarab focus in East Azarbaijan province where fourteen samples of Y. pestis were isolated from M. persicus, M. vinogradovi, and Mesocricetus auratus and from their fleas; Xenopsylla conformis and Nosopsylla iranus iranus [80]. The Y. pestis strains isolated from the M. persicus in the Trans-Arax focus in Armenia were characterized by higher virulence than those that are isolated from voles in the Transcaucasus Mountainous focus[81].

In a recent serological survey carried out by Esmaeili et al., in Western Iran antibodies against Y. pestis F1 capsular antigen were detected in a M. persicus [22]. Whether Y. pestis strains lacking the F1 antigen naturally occur in Iran is not known but could lead to an underestimation of the current seroprevalence.

Meriones species notably M. persicus were reported to be main reservoir host for pathogens rather than bacterium Y. pestis. In the parasitological studies sandfly-borne Leishmania spp. including L. major [82], L. infantum [83] and L. donovani [84] were isolated from M. persicus specimens. Meriones species rather than M. persicus (M. libycus and M. hurrianae) have been reported as the major reservoir host of zoonotic cutaneous leishmaniasis in several endemic areas of Iran [85-89]. The endoparasites ranging from Acanthocephala to Cestoda and Nematoda were identified in M. persicus as well [90]. These findings place the Persian jird and the Xenopsyllinae as the major vertebrate and vector hosts of flea-borne diseases in Iran including Y. pestis, the etiological agent of plague.

Indeed, Xenopsylla spp. were collected from 18 provinces with a wide array of climatic conditions ranging from cold mountainous areas to warm and dry sandy plains and deserts (Table 1).

Most species of the Pulicidae family are notorious vectors of disease agents causing plague, murine typhus, and tularemia but also transmit helminths. Several species of the Xenopsylla genus play an important role in the transmission of Y. pestis, the etiological agent of plague, from rodents to human [91]; the most classical and significant vector being X. cheopis [92].

Indeed, X. cheopis accounts for 80% of the fleas collected off rodent hosts in the natural endemic plague foci of Iran [93]. X. cheopis is also the vector of various human pathogenic Bartonella species [6, 94]. The cat scratch disease, caused by B. henselae, has been considered as an emerging zoonotic bacterial pathogen in veterinary and human medicine. Cats are the basic source of the bacteria. Bacteria are transferred from cat to cat by the flea Ctenocephalides felis, another cosmopolitan flea, which have been reported in the Iranian cat population [95]. Murine typhus or endemic typhus caused primarily by Rickettsia typhiis another rodent-borne disease that is transmitted to humans by the flea X. cheopis [96]. Pulex irritans and Nosopsyllus fasciatus are secondary vectors of murine typhus Rickettsia [97] that is endemic through coastal regions of the Caspian Sea and the Persian Gulf [98].

Rickettsia felis is the cause of another flea-borne “spotted fever group” rickettsiosis. R. felis is transmitted by the bite or faeces of several flea species, and transovarially in Ctenocephalides felis felis (and the African subspecies C. f. strongylus) but also in C. orientis present in Iran, so that they are considered as vectors and reservoir hosts of this pathogen [99].

Ctenocephalides felis, C. canis- that have been collected from the studied areas extensively (Table 1)—and P. irritans are the intermediate hosts of flatworms such as Dipylidium caninum, or nematodes as the filaria Acanthocheilonema reconditum. Hence dog, cat and rarely human infection occurs following ingestion of infected fleas [100-101]. Typically, a human is bitten more often by a cat flea (C. felis) than a dog flea (C. canis) which is very or even monospecific. Cosmopolitan fleas as helminths vector have less medical than veterinary importance, since the helminth species they transmit rarely infest humans and are virtually harmless.

Nosopsyllus fasciatus, a Ceratophyllidae and Coptopsylla lamellifer, a Coptopsyllidae, were collected in 14 different regions of Iran. They play a role in enzootic plague cycles, that is in circulating the plague bacterium Y. pestis between rodents but since they do not readily bite humans in a natural setting, are only accidental vectors of Y. pestis to humans exposed [38, 41, 102–103].

Fleas are also considered vectors of F. tularensis the etiological agent of tularemia [104]. Vulnerable animals such as hares and rodents frequently die in large numbers during epizootics. Human infections take place through several routes, including insect bites and direct contact to an infected animal. It can affect the skin, eyes, lymph nodes, lungs and, less often, other internal organs. According to recent studies (which have shown the presence of this disease in western and eastern regions of Iran) and the previous studies (which have shown the presence of this disease in the east and north-west of the country [105]), the possibility of transmission of this agent by fleas should be considered in all parts of the country [106].

Most leptopsyllids parasitize rodents and a few birds. Species of Frontopsylla, Leptopsylla, Mesopsylla, Ophthalmopsylla and Paradoxopsyllus are known as main or suspected vectors of plague, murine typhus, erysipeloid, listeriosis and salmonellosis in the Central Asia[107]. In an experiment it was showed that L. segnis is more successful in transmitting R. typhi to rats than X. cheopis [64]. Leptopsylla aethiopica aethiopica which transmits plague in Africa recently have been reported from Semnan province [50]; however its presence and identity in the region is very questionable.

People who travel to rural areas should consciously avoid flea bites especially in populations camping outside (herders, travelers, nomads) and avoid exposure to wild rodents and their fleas. In domestic areas, in order to prevent bites and thus disease transmission to humans, the floors and walls, as well as the rodents’ burrows around settlements, should theoretically be sprayed with insecticides. A few days later the application of rodenticides is necessary.

There were virtually no records of some flea species in a few provinces like North Khorasan (Fig 1). This is mainly due to inadequate inventories, especially in remote areas, or minorly due to the changing of geographical boundaries where the number of provinces in old classification has increased from 10 to 31 provinces.

In this paper we highlighted the geographical gaps on the Siphonaptera fauna of Iran. Generally, it shows that extensive fundamental and systematic research is still needed to determine the impact of off-host abiotic conditions and host identity (either mammal or bird) on host specificity, and on the potential for flea-borne diseases spread and transmission risk.

Co-evolution partly explains host-flea relationships which are translated into various degrees of host specificity (as shown in Tables 4–7) and morphological adaptations of the parasite [108]. Host specificity is important from the perspective of transmission of disease agents. It is more probable that, vertebrate hosts with related taxonomy or similar ecologies will have flea species that share similar pathogens. Depending on the level of infestation, flea species do not cause major problem to their hosts [108]. While some fleas species, virtually exclusively females, (Echidnophaga spp., Vermipsylla spp., Dorcadia spp., Tunga spp), spend much of their adult lives embedded or fixed in the host skin, this is far from being the rule. Indeed, most species jump on a host to feed intermittently before returning to the host dwelling place, usually a nest or burrow [6].

Den/nest making hosts (mammals or birds) display a more specific flea fauna than non roosting species [6]. It has been shown that fleas possibly appeared with mammals and speciated with rodents which still have the most speciose extant fauna (74%)[109].

Since rodent-borne, bat-borne and vector-borne diseases are the major rising concerns to health authorities, and threats to public health making inventories of the host and their ectopoarasitic fauna has become as never before a priority. Although most flea-borne diseases are not classified in the 17 neglected tropical diseases (NTDs) list made by the World Health Organization, this doesn’t mean those are unimportant or not causing an underestimated morbidity burden worldwide. The lack of recognition by major stakeholders, and the local lack of diagnostic tools and awareness are impeding improvements into flea-borne disease research. However, with about seven human or zoonotic highly pathogenic agents circulating among -possibly- the 117 flea species throughout Iran, there is an urgent need to organize and fund flea-host-pathogen ecological surveys in the face of rapid environmental and human behavioral changes.

Conclusion

The first step in identifying the risk linked to flea exposure is to make a list of the species before any public health measures can be taken. Flea-borne diseases are caused by emerging and re-emerging infectious agents which distribution, prevalence and incidence are currently increasing. However, the data about fleas and their medical significance in different geographical regions of Iran is limited. We took the first step in this paper but supplementary studies are required to i) complete the list, especially in areas where there are no reportsor poor faunistic studies and ii) perform molecular screening of flea pools in order to detect specific pathogen circulation in domestic fauna and wildlife in order to prevent future epidemics.