During this study, 284 individuals of rodents belonging to 17 species were trapped in 38 locations distributed in northeast of Iran, including Apodemus witherbeyi, Mus musculus, Nesokia indica, Rattus norvegicus, Rattus pytoris, Meriones libycus, Meriones persicus, Rhombomys opimus, and Tatera indica, (Muridae), Cricetulus migratorius, Ellobius fuscocapillus, Microtus paradoxus, and Microtus transcaspicus (Cricetidae), Calomyscus elburzensis and Calomyscus hotsoni (Calomyscidae), Scaratus elater (Dipodidae), and Spermophilus fulvus (Sciuridae). The highest capture success was recorded for Meriones persicus (43 out of 284: 15.1%) followed by Mus musculus (30 out of 284: 10.5%), while the lowest capture success was recorded for Rhombomys opimus and Rattus pyctoris both with 0.3% (1 out of 284).
The highest number of captured rodents was recorded from Sangbast (Razavi Khorasan: Mashhad-Torbat road) (39 specimens out of 284: 13.7%), and the lowest number was recorded from Robat-e mahi (Razavi Khorasan: Sarakhs) and Kahoo and Golbahar (Razavi Khorasan), all with 0.3% (1 specimens out of 284). Although, the number of rodent species (diversity of hosts) in Sangbast and Soltanabad (Razavi Khorasan: Chenaran) was higher than in the rest of sampling sites (6 out of 17 rodent species: 35.2%). In contrast, Baba Ramezan (Kalat), Chenaran, Firouzabad (Mashhad), Golbahar, Kahoo, Robat-e mahi, Tirgan (Dargaz) in Razavi Khorasan and Qaen, Sarayan, and Shadan and Olang heights (Birjand) in South Khorasan showed the lowest number and diversity in the captured rodent's species with only one captured species (5.8%).
The rocky areas were strongly dominated by Meriones persicus and public areas by Mus musculus and Rattus norvegicus. Ellobius fuscocapillus and Microtus transcaspicus were dominant captured species in the grasslands and parks, respectively, while the meadows and sandy soils were both dominated by Tatera indica and Spermophilus fulvus.
Only one individuals (out of 284: 0.3%) was infested with all four groups of ectoparasitic. Moreover, four (1.4%) and five (1.7%) individuals harboring three and two groups of ectoparasites, respectively. A total of 275 individuals (96.8%) were parasitized by only one ectoparasite group. Hence, among the infested animals, 133 out of 143 (93%) specimens of rodents were noted to carry only one group of ectoparasites, while only 10 out of 143 (approximately 7%) specimens of rodents were noted to carry more than one group of ectoparasites.
Overall infestation rate was 50.3% (143 out of 284). The infestation rate with fleas, lice, ticks and mites were 58.7%, 30%, 13.2% and 9%, respectively. Fleas with five known and three unknown species, belonging to three genera, were the most diverse and prevalent group (29.5%), followed by lice (15.1%), while the lowest prevalence was observed in the mites group (4.5%), and followed by ticks (6.6%). Ticks group with two genera, including two known and two unknown species, showed the lowest diversity (Table 1).
Table 1
List of collected ectoparasites parasitized rodents captured from northeastern Iran
Order | Family | Species |
Siphonaptera (fleas) | Ceratophyllidae Dampf, 1908 | Ctenophthalmus pseudagyrtes Baker, 1904 |
Ctenophthalmus sp. |
Nosopsyllus fasciatus (Bosc, 1801) |
Nosopsyllus iranus Wagner and Argyropulo, 1934 |
Nosopsyllus sp. |
Pulicidae Billberg, 1820 | Xenopsylla buxtoni Jordan, 1949 |
Xenopsylla cheopis (Rothschild, 1903) |
Xenopsylla sp. |
Phthiraptera (lice) | Hoplopleuridae Ewing, 1929 | Hoplopleura captiosa Johnson, 1960 |
Polyplacidae Fahrenholz, 1912 | Polyplax asiatica Ferris, 1923 |
Polyplax gerbilli Ferris, 1923 |
Polyplax paradoxa (Johnson, 1960) |
Polyplax spinulosa (Burmeister, 1839) |
Ixodida (ticks) | Ixodidae C. L. Koch, 1844 | Haemaphysalis punctata Canestrini and Fanzago, 1878 |
Haemaphysalis sp. |
Ixodes trianguliceps Birula, 1895 |
Ixodes sp. |
Mesostigmata (mites) | Hirstionyssidae Evans and Till, 1966 | Hirstionyssus meridianus Zemskaja, 1955 |
Laelapidae Berlese, 1892 | Haemolaelaps sp. |
Laelaps algericus Hirst, 1925 |
Laelaps sp. |
Trombidiformes (mites) | Trombiculidae Ewing, 1929 | Microtrombicula sp. |
Spermophilus fulvus showed the highest mean intensity (0.52), followed by Nesokia indica (0.37). Mean intensity about 0.3 was recorded for three species Cricetulus migratorius, Meriones persicus and Mus musculus. Due to showing no infestation, the lowest intensity with the value of zero belonged to Calomyscus hotsoni and Scaratus elater. Other rodent species including Apodemus witherbeyi, Calomyscus elburzensis, Ellobius fuscocapillus, Meriones libycus, Microtus paradoxus, Microtus transcaspicus, Rattus norvegicus, Rattus pyctoris, Rhombomys opimus, and Tatera indica showed intensity value of 0.25. Detailed information is presented in Table 2.
Table 2
List of captured rodents together with their ectoparasite assemblage. For each host species, the numbers of captured and overall infested individuals are provided in parenthesis, respectively
Host Species | Parasitic flea | Parasitic louse | Parasitic tick | Parasitic mite |
Apodemus witherbeyi (19, 7) | - | - | Haemaphysalis sp., Ixodes sp. | - |
Calomyscus elburzensis (4, 4) | Nosopsyllus iranus | - | - | - |
Calomyscus hotsoni (7, 0) | - | - | - | - |
Cricetulus migratorius (24, 9) | Nosopsyllus iranus | Polyplax asiatica | - | - |
Ellobius fuscocapillus (23, 4) | - | - | - | Haemolaelaps sp. |
Meriones libycus (17, 7) | Nosopsyllus fasciatus | - | - | Hirstionyssus sp. |
Meriones persicus (43, 33) | Nosopsylla fasciatus, Nosopsyllus iranus, Xenopsylla buxtoni, Xenopsylla cheopis | Polyplax asiatica, Polyplax paradoxa | Ixodes trianguliceps, Haemaphysalis punctata | Haemolaelaps sp. |
Microtus paradoxus (3, 3) | Nosopsyllus fasciatus | - | - | - |
Microtus transcaspicus (20, 8) | Nosopsyllus fasciatus, Xenopsylla buxtoni | - | - | - |
Mus musculus (30, 16) | Ctenophthalmus sp., Nosopsyllus fasciatus, Nosopsyllus iranus | Hoplopleura captiosa | Haemaphysalis punctata, Haemaphysalis sp. | Haemolaelaps sp., Laelaps algericus, Laelaps sp., Microtrombicula sp. |
Nesokia indica (20, 16) | Nosopsylla fasciatus, Nosopsylla sp., Xenopsylla cheopis, Xenopsylla sp. | Hoplopleura captiosa, Polyplax asiatica | Haemaphysalis punctata | - |
Rattus norvegicus (26, 15) | Ctenophtalmus pseudagyrtes, Ctenophtalmus sp., Nosopsyllus fasciatus, Xenopsylla buxtoni, Xenopsylla cheopis | Hoplopleura captiosa, Polyplax gerbilli, Polyplax spinulosa | - | - |
Rattus pyctoris (1, 1) | Xenopsylla buxtoni | - | - | - |
Rhombomys opimus (1, 1) | Nosopsyllus fasciatus | - | - | - |
Scaratus elater (3, 0) | - | - | - | - |
Spermophilus fulvus (25, 12) | Nosopsylla fasciatus | Polyplax asiatica | - | - |
Tatera indica (18, 7) | Xenopsylla buxtoni | Polyplax gerbilli | - | - |
A total of 178 specimens of ectoparasites from five orders Siphonaptera (89 specimens), Phthiraptera (57 specimens), Ixodida (19 specimens), Mesostigmata (12 specimens) and Trombidiformes (1 specimens) were collected and identified from the infested hosts. This can be further categorized into three, two, two and four genera of flea, louse, tick and mite, respectively including Ctenophthalmus pseudagyrtes, Ctenophthalmus sp., Nosopsyllus fasciatus, Nosopsyllus iranus, Nosopsyllus sp., Xenopsylla buxtoni, Xenopsylla cheopis, and Xenopsylla sp. (fleas: Siphonaptera), Hoplopleura captiosa, Polyplax asiatica, Polyplax gerbilli, Polyplax paradoxa, and Polyplax spinulosa (sucking lice: Phthiraptera), Haemaphysalis punctata, Haemaphysalis sp., Ixodes trianguliceps, and Ixodes sp. (ticks: Ixodida), and Haemolaelaps sp., Hirstionyssus meridianus, Laelaps algericus, and Laelaps sp. (mites: Mesostigmata), and Microtrombicula sp. (mites: Trombidiformes) (Table 1).
Of the parasitic fleas and lice, Nosopsyllus fasciatus (Ceratophyllidae) and Polyplax asiatica (Polyplacidae) were dominated (50.5% and 52.6% of all fleas and lice, respectively). For tick and mite groups, Haemaphysalis punctata (Ixodidae) (36.84%) and Haemolaelaps sp. (Laelapidae) (61.5%) were recorded as the most abundant sampled ectoparasites.
The values of abundance and infestation with ectoparasites groups varied between host species and sampling locations. Mus musculus had the most diverse ectoparasite assemblage (10 ectoparasite species) followed by Meriones persicus (9 ectoparasite species), Rattus norvegicus (8 ectoparasite species) and Nesokia indica (7 ectoparasite species), suggesting that these species can accommodate variety of ectoparasites (Table 2). In contrast, Calomyscus hotsoni and Scaratus elater carried no ectoparasite.
The two most commonly found ectoparasite species were Nosopsyllus fasciatus (45 out of 178 specimens: 25.2%) and Polyplax asiatica (30 out of 178 specimens: 16.8%). The flea Nosopsyllus fasciatus exhibited low host specificity, infesting diverse species of rodents (52.9%: 9 out of 17 rodent species including Meriones libycus, Meriones persicus, Microtus paradoxus, Microtus transcaspicus, Mus musculus, Nesokia indica, Rattus norvegicus, Rhombomys opimus and Spermophilus fulvus). The louse Polyplax asiatica was found on 4 out of 17 rodent species (23.5%), exhibiting moderate host specificity evident by infesting Cricetulus migratorius, Meriones persicus, Nesokia indica, and Spermophilus fulvus. Among the known species of ectoparasite, the flea Ctenophthalmus pseudagyrtes was only recorded in Rattus norvegicus, and the lice species Polyplax paradoxa and Polyplax spinulosa were only found on Meriones persicus and Rattus norvegicus, respectively. The tick Ixodes trianguliceps was also collected only from Meriones persicus and the mite Laelaps algericus from Mus musculus. Thus, each of these five ectoparasite species showed high host specificity (1 out of 17 rodent species: 5.8%) (Table 3). Hence, nine known species of ectoparasites (around 64.2%) shared more than one host and approximately 35.7% of them (n = 5 out of 14) were singletons.
Table 3
Host selection in ectoparasite assemblage collected from northeastern Iran; list of collected ectoparasites showing high host specificity in association with the rodent which they hosted
Ectoparasitic group | Ectoparasite species | Host |
Flea | Ctenophtalmus pseudagyrtes | Rattus norvegicus |
Nosopsylla sp. | Nesokia indica |
Xenopsylla sp. |
Lice | Polyplax paradoxa | Meriones persicus |
Polyplax spinulosa | Rattus norvegicus |
Tick | Ixodes trianguliceps | Meriones persicus |
Ixodes sp. | Apodemus witherbeyi |
Mite | Laelaps algericus | Mus musculus |
Laelaps sp. |
Microtrombicula sp. |
Hirstionyssus sp. | Meriones libycus |
Of the parasitic fleas, Nosopsyllus fasciatus was dominant species, found in 19 out of 37 sampling localities (51.3%). In contrast, Ctenophthalmus pseudagyrtes was only recorded from Faruj in North Khorasan (2.7%). Among lice, Polyplax asiatica was considered as the most common species (11 out of 37: 29.7%), while Polyplax spinulosa and Polyplax gerbilli were reported as the rarest one (5.4%), both were only recorded from Faruj and Mashhad-Torbat road (Razavi Khorasan). Of the tick group, genus Haemaphysalis showed dominancy as compared with genus Ixodes (21.6% vs. 16.2%), found in eight and six sampling localities, respectively. Last, members of the genus Haemolaelaps was the most common mite (3 out of 37: 8.1%). In contrast, each of the mite species Laelaps algericus and Hirstionyssus meridianus as well as two unknown species Laelaps sp. and Microtrombicula sp. were only found in one locality (2.7%) (Figs. 3, 4).
Species Nosopsyllus fasciatus was recorded as a common flea for most of the sampling habitats (7 out of 10: 70%), but species Ctenophthalmus pseudagyrtes, found from public areas, was unique for its respective habitat (10%). Lice species Polyplax asiatica and Hoplopleura captiosa were found in half of the habitat types (50%), although Polyplax paradoxa (recorded from grassland and rocky areas) and Polyplax spinulosa (reported from meadows and public areas) were the less common lice species, both found in only two habitat types (each with 20% frequency). Among tick group, genus Ixodes was the most common tick found in four habitat types (40%). However, Ixodes trianguliceps was only captured from rodents inhabit rocky areas (10%). Mite genus Laelaps was recorded as the most common mite found in 30% of habitat types. In contrast, Laelaps algericus, Hirstionyssus meridianus and Microtrombicula sp. were only found in farms and gardens, sandy soils, and public areas, respectively (each with 10% frequency). Detailed information is presented in Table 4.
Table 4
Spatial distribution of ectoparasites on rodents trapped in different habitats in northeastern Iran
Habitat type | Host Species | Parasitic flea | Parasitic louse | Parasitic tick | Parasitic mite |
Farm and garden | Apodemus witherbeyi, Cricetulus migratorius, Meriones libycus, Mus musculus, Rattus norvegicus | Ctenophthalmus sp., Xenopsylla buxtoni, Xenopsylla cheopis | - | Ixodes sp. | Laelaps algericus |
Forest | Calomyscus hotsoni, Mus musculus, Spermophilus fulvus | - | - | - | - |
Grassland | Apodemus witherbeyi, Cricetulus migratorius, Ellobius fuscocapillus, Meriones libycus, Meriones persicus, Microtus transcaspicus, Mus musculus, Rattus norvegicus, Spermophilus fulvus | Nosopsyllus fasciatus, Nosopsyllus iranus, Xenopsylla buxtoni, Xenopsylla cheopis | Polyplax paradoxa | Ixodes sp. | Haemolaelaps sp. |
Meadow | Apodemus witherbeyi, Ellobius fuscocapillus, Meriones libycus, Mus musculus, Nesokia indica, Rattus norvegicus, Rhombomys opimus, Spermophilus fulvus, Tatera indica | Nosopsyllus fasciatus, Nosopsyllus iranus, Xenopsylla sp. | Hoplopleura captiosa, Polyplax asiatica, Polyplax gerbilli, Polyplax spinulosa | Haemaphysalis sp. | - |
Park | Ellobius fuscocapillus, Microtus transcaspicus, Mus musculus, Nesokia indica | Nosopsyllus fasciatus | Hoplopleura captiosa, Polyplax asiatica | - | Haemolaelaps sp., Laelaps sp. |
Public area | Meriones libycus, Mus musculus, Nesokia indica, Rattus norvegicus, Spermophilus fulvus | Ctenophtalmus pseudagyrtes, Nosopsylla fasciatus, Nosopsyllus iranus, Xenopsylla buxtoni, Xenopsylla cheopis | Hoplopleura captiosa, Polyplax asiatica, Polyplax spinulosa | Haemaphysalis punctata | Haemolaelaps sp., Laelaps sp., Microtrombicula sp. |
Rocky area | Apodemus witherbeyi, Calomyscus elburzensis, Calomyscus hotsoni, Cricetulus migratorius, Meriones libycus, Meriones persicus, Microtus paradoxus, Microtus transcaspicus, Mus musculus, Nesokia indica, Rattus norvegicus, Rattus pyctoris | Ctenophtalmus sp., Nosopsyllus fasciatus, Nosopsyllus iranus, Xenopsylla buxtoni, Xenopsylla cheopis | Hoplopleura captiosa, Polyplax asiatica, Polyplax paradoxa | Haemaphysalis punctata, Haemaphysalis sp., Ixodes trianguliceps, Ixodes sp. | Haemolaelaps sp. |
Sandy soil | Meriones libycus, Mus musculus, Nesokia indica, Scaratus elater, Spermophilus fulvus, Tatera indica | Nosopsylla fasciatus, Nosopsyllus iranus, Nosopsylla sp., Xenopsylla buxtoni | Hoplopleura captiosa, Polyplax asiatica, Polyplax gerbilli | Haemaphysalis punctata, Haemaphysalis sp. | Hirstionyssus sp. |
Semi-desert | Meriones libycus, Tatera indica | Xenopsylla buxtoni | Polyplax gerbilli | - | - |
Woodland | Apodemus witherbeyi, Ellobius fuscocapillus, Meriones persicus, Mus musculus | Nosopsyllus fasciatus | - | Ixodes sp. | - |
Parasitism interaction and seasonality
Seasonal fluctuations were found in the occurrence of ectoparasite, with remarkable differences according to flea species; fleas were more abundant in spring (50 collected flea specimens in springs out of 89 in other seasons: 56.1%). Lice were more common in winter (19 out of 57: 33.3%), and ticks demonstrated high abundance with equal value in spring and summer (6 out of 19: 31.5%) decreasing in numbers as the season progressed. Last, mites showed a high abundance in the autumn (7 out of 13: 53.8%). Fleas, lice and ticks were recorded in all sampling months, while members of mite group had no record in the summer.
Flea species Nosopsyllus fasciatus was reported with most records in all sampling months (mean intensity 0.38, 0.68, 0.66, and 0.76 in spring, summer, autumn, and winter, respectively). Louse species Polyplax asiatica showed the highest mean intensity among other lice species in spring (0.85), summer (0.38), and winter (1), while Hoplopleura captiosa was recorded as the most common lice species in the autumn (0.6). Tick species Haemaphysalis punctata was more common in spring and autumn (mean intensity 0.5 and 0.75, respectively), while Ixodes sp. and Ixodes trianguliceps showed the highest mean intensity (with value of 0.66 for each one) in the summer and winter, respectively. Finally, mite Haemolaelaps sp. with most records in the spring and autumn showed mean intensity 0.75 and 0.71, respectively, while species Hirstionyssus meridianus, which was recorded exclusively in the winter, along with Laelaps sp. were the most common lice in winter, each with mean intensity 0.5 (Table 5).
Table 5
Temporal (seasonal) distribution of ectoparasites parasitized rodents in northeastern Iran. The number given in parenthesis show the number of collected ectoparasite
Capturing season | Parasitic flea | Parasitic louse | Parasitic tick | Parasitic mite |
Spring | Ctenophthalmus sp. (1), Nosopsyllus fasciatus (18), Nosopsyllus iranus (12), Xenopsylla buxtoni (6), Xenopsylla cheopis (13) | Hoplopleura captiosa (1), Polyplax asiatica (12), Polyplax paradoxa (4) | Ixodes trianguliceps (1), Haemaphysalis punctata (3), Haemaphysalis sp. (2) | Haemolaelaps sp. (3), Laelaps algericus (1) |
No. of rodents infected by flea: 47 | No. of rodents infected by louse: 14 | No. of rodents infected by tick: 6 | No. of rodents infected by mite: 4 |
Summer | Ctenophtalmus pseudagyrtes (1), Ctenophtalmus sp. (1), Nosopsyllus fasciatus (11), Nosopsyllus iranus (2), Xenopsylla buxtoni (2) | Hoplopleura captiosa (2), Polyplax asiatica (5), Polyplax gerbilli (4), Polyplax paradoxa (3), Polyplax spinulosa (1) | Haemaphysalis punctata (1), Ixodes trianguliceps (1), Ixodes sp. (4) | - |
No. of rodents infected by flea: 16 | No. of rodents infected by louse: 13 | No. of rodents infected by tick: 6 | No. of rodents infected by mite: 0 |
Autumn | Nosopsylla fasciatus (6), Nosopsyllus iranus (1), Nosopsylla sp. (1), Xenopsylla buxtoni (2) | Hoplopleura captiosa (3), Polyplax asiatica (2), Polyplax gerbilli (1) | Haemaphysalis punctata (3), Haemaphysalis sp. (1) | Haemolaelaps sp. (5), Laelaps sp. (1), Microtrombicula sp. (1) |
No. of rodents infected by flea: 9 | No. of rodents infected by louse: 5 | No. of rodents infected by tick: 4 | No. of rodents infected by mite: 7 |
Winter | Nosopsylla fasciatus (10), Nosopsyllus iranus (1), Xenopsylla sp. (1) | Hoplopleura captiosa (4), Polyplax asiatica (11), Polyplax gerbilli (1), Polyplax spinulosa (3) | Haemaphysalis sp. (1), Ixodes trianguliceps (2) | Hirstionyssus sp. (1), Laelaps sp. (1) |
No. of rodents infected by flea: 13 | No. of rodents infected by louse: 11 | No. of rodents infected by tick: 3 | No. of rodents infected by mite: 2 |
Parasitism interaction and host sexuality
Distribution of ectoparasite was also affected by host sex which is called sex-biased parasitism. Overall prevalence of four groups of ectoparasite on male rodents in comparison with females was recorded (56.4% vs. 44.4%). However, similar mean intensity values were detected for both sexes (1.21 in males and 1.28 in females). Flea Nosopsyllus fasciatus, louse Polyplax asiatica and ticks of genus Haemaphysalis were the most abundant ectoparasite, among other members of their relevant group, in both male and female rodents. Although genus Haemolaelaps was the most abundant mite parasitized male hosts, but members of two genera Haemolaelaps and Laelaps showed equal abundance on females.
Host age is another trait which could have effect on the ectoparasite assemblage parasitizing hosts. Overall prevalence of four groups of ectoparasite on mature hosts was greater in comparison with immature ones (approximately 51% vs. 47%). In contrast, the mean intensity values of 1 and 1.34 were recorded for mature and immature rodent hosts, respectively (Table 6).
Table 6
Age-biased parasitism of rodents host harboring different groups of ectoparasite in northeastern Iran
Host age | No. of captured rodent | No. of infected rodent | Prevalence of infection | Mean intensity of infection |
Immature | 49 | 23 | 46.9% | 1.34 |
Mature | 235 | 120 | 51% | 1 |
Total | 284 | 143 | | |
Manifestation of sexual differences in ectoparasite infestation was different among male and female hosts between seasons. In spring, the prevalence of overall infection for males and females were 65.4% and 57.1%, respectively. Likewise, nearly similar values of prevalence were recorded for males (44.1%) and females (44%) in winter. In contrast, male-biased parasitism was found in summer and autumn; prevalence in males was at about four times the value recorded for females (74.1% vs. 17.5%) in summer, and during the autumn, this was about 1.5 times (60% vs. 36.6%).
Among all sampling localities, the highest prevalence (100%) was recorded for Robat-e mahi (Razavi Khorasan province), Faruj, Bojnourd, Shirvan, Shirvan-Bojnourd road, and Siman Factory (North Khorasan province), and Qaen, Birjand, Sarayan, Nehbandan, Ferdows (South Khorasan province). In contrast, the lowest prevalence with the value of zero was recorded for Baba Ramezan, Chenaran, Golbahar, Kahoo, and Tirgan in Razavi Khorasan province, and Shadan and Olang heights in South Khorasan province.
Among habitats which monitored for capturing rodents, semi-deserts, followed by farms and gardens, and also rocky areas showed the highest prevalence of ectoparasites (66.6%, 62.5%, and 61%, respectively). The lowest prevalence was recorded for the forest, may be due to sampling error and capturing no rodents there. The mean intensity of the flea infection was highest in the rocky areas (0.74), grasslands (0.63), and farms and gardens (0.6), while louse infection showed the highest value for mean intensity in meadows (0.66), sandy soils (0.66), and public areas (0.6). Same mean intensity of infection of flea and louse was reported from parks and semi-deserts (0.5), but woodlands had same intensity for flea and tick (0.5).