Chewing lice of wild birds in Iran: new data and a checklist of avian louse species reported in Iran

Between September 2019 and December 2023, a total of 612 wild birds representing 16 orders, 33 families, 60 genera, and 78 species from nine provinces of Iran with different climates namely Hamedan (n = 54), Sistan-va-Baluchestan (n = 372), Kerman (n = 73), South Khorasan (n = 52), Mazandaran (n = 7), Chaharmahal-va-Bakhtiari (n = 2), Gilan (n = 2), Golestan (n = 18), North Khorasan (n = 9), and Razavi Khorasan (n = 23) were examined for chewing lice infestation. Naked eye examination revealed that 58 birds (9.5%) were infested with at least one chewing louse species. Collected lice specimens belonged to 28 species from the families Philopteridae, Menoponidae and Laemobothriidae including Strigiphilus strigis (n = 55, 15.6%), Falcolipeurus quadripustulatus (n = 41, 11.6%), Craspedorrhynchus platystomus (n = 40, 11.3%), Colpocephalum turbinatum (n = 36, 10.2%), Laemobothrion maximum (n = 25, 7.1%), Nosopon lucidum (n = 20, 5.6%), Degeeriella fulva (n = 18, 5.1%), Colpocephalum eucarenum (n = 16, 4.5%), Laemobothrion vulturis (n = 15, 4.2%), Anaticola crassicornis (n = 13, 3.7%), Craspedorrhynchus aquilinus (n = 9, 2.5%), Degeeriella fusca (n = 7, 2.0%), Aegypoecus trigonoceps (n = 7, 2.0%), Quadraceps obscurus (n = 6, 1.7%), Colpocephalum impressum (n = 6, 1.7%), Trinoton querquedulae (n = 6, 1.7%), Colpocephalum heterosoma (n = 5, 1.4%), Colpocephalum nanum (n = 5, 1.4%), Lunaceps holophaeus (n = 4, 1.1%), Quadraceps spp. (n = 4, 1.1%), Actornithophilus uniseriatus (n = 2, 0.6%), Nosopon chanabense (n = 2, 0.6%), Actornithophilus cornutus (n = 1, 0.3%), Cuclotogaster heterographus (n = 1, 0.3%), Falcolipeurus suturalis (n = 1, 0.3%), Laemobothrion atrum (n = 1, 0.3%), Colpocephalum gypsi (n = 1, 0.3%), and Rallicola cuspidatus (n = 1, 0.3%). All of these species except six, i.e., Trinoton spp., C. aquilinus, L. vulturis, L. maximum, C. impressum, C. turbinatum, and C. heterographus are recorded for the first time from Iran. This study is the largest epidemiological study to date performed in the country. Data reported herein contribute to our knowledge about diversity of avian chewing lice from wild birds in Iran. In this paper, an updated checklist of louse species reported from Iran according to their avian hosts is presented.


Introduction
Lice are small (0.35-11 mm long as adults), wingless, dorsoventrally flattened insects.They are obligatory, permanent ectoparasites of birds and mammals throughout the world which typically, parasitize individuals in small numbers and cause no apparent discomfort however, some of the lice can cause skin lesions and act as vectors or intermediate hosts of several bacteria, viruses and filarial parasites (1,2).In addition, it has been shown that Piagetiella titan infesting white pelicans may invade the oral cavity causing erosions and petechial hemorrhages (3)(4)(5).
Lice (Insecta: Psocoptera: Phthiraptera) with about 5,000 known species, present on roughly 4,000 species of birds and 800 mammals, are categorized in four suborders (6).Species of the suborder Anoplura have adopted to suck blood from capillaries of mammals and ingest it, while Amblycera, Ischnocera, and Rhynchophthirina (formerly known as Mallophaga) have chewing mouth pieces, adapted to eat hairs and feathers, and sometimes also the skin and blood of birds and mammals (7).Avian chewing lice belong to one of two sub-orders: Amblycera, which occur on feathers and skin, or Ischnocera, which are more restricted to feathers (1).Most of the lice species are strongly associated with hosts, their phylogeny parallels that of hosts, sometimes with different speeds however, "host specificity" cannot be assumed (7,8).Among different fields of wildlife parasitology, studying avian chewing lice is important as their epizootiology is largely associated with geographical distribution of their hosts.
Iran is a country in western Asia with a territory of 1,648,195 km 2 .It is the second largest country in the Middle East and the 17th largest in the world.In the country, 550 avian species are distributed which is almost equal to the richness of birds in Europe (9,10).However, there is limited and scanty information about their parasites fauna specially the chewing lice (11)(12)(13)(14) with several published in Persian language and presented in local congresses (15)(16)(17)(18)(19). Considering the scarcity of published records of lice in Iran, we aimed to gather new data and present an updated checklist of birds' Phthiraptera occurring in the country.
We also collected all the available information about chewing lice infesting birds in Iran.The databases and search engines employed for the literature review were Phthiraptera.info, 1 PubMed, 2 Google, 3  Scientific Information Database of Iran, 4 the collection of defended theses at all Iranian Universities, 5 and the collection of proceedings of Iranian congresses. 6Valid names of the louse and bird species were obtained from Global Biodiversity Information Facility resources (36).
In Supplementary Table 1, the information in Table 1 in addition to world conservation status according to International Union for Conservation of Nature (IUCN) and names of birds in Persian language are presented.

Discussion
This study is the largest epidemiological study to date performed in Iran.However, low number of collected lice from birds could be due to the fact that most of the ectoparasites including lice leave dead hosts rather quickly.Data reported herein contribute to our knowledge about diversity of avian chewing lice from wild birds in Iran and in a broader context in western Asia.Lice species in this study belonged to both Ischnocera (15 species), Amblycera (14 species).We compiled our data and previous information about avian lice species in Iran in Table 2.So far, lice infestation of birds belonging to 16 orders, 33 families, 60 genera, and 78 species and subspecies has been recorded from Iran.In Supplementary Table 2, the information in Table 2 in addition to world conservation status and names of birds in Persian language are presented.
Review of all relevant publications indicated that in some reports from Iran, researchers identified the lice specimens only to genus level, i.e., Brueelia (nine documents), Philopterus, Menacanthus (six documents), Ricinus, Lipeurus (three documents), Sturnidoecus, Trinoton, Menopon, and Goniodes (two documents), Ardeicola, Colpocephalum, Craspedorrhynchus, Laemobothrion, Strigiphilus, and Myrsidea (one document) (14,16,17,19,38,40,47,50,51,62).The reason could be damage of the specimens, observation of a louse with morphological differences from identification keys or difficulty in identification of the species.It is necessary that researchers will try their best to identify the lice to species level correctly and provide the drawings, measurements, or photos.
This study provides the first information about lice infestation of wild birds in different regions of Iran and reports Craspedorrhynchus platystomus, Colpocephalum nanum, Colpocephalum gypsi, Colpocephalum eucarenum, Colpocephalum heterosoma, Degeeriella fulva, Degeeriella fusca, Nosopon chanabense, Nosopon lucidum, Falcolipeurus quadripustulatus Falcolipeurus suturalis, Aegypoecus trigonoceps, Trinoton querquedulae, Anaticola crassicornis, Quadraceps obscurus, Rallicola cuspidatus, and Strigiphilus strigis for the first time from the country.Review of the published data on avian lice fauna of Iran shows that the information is available for almost 14% of the bird species.In contrast, researchers from the neighboring country Turkey have identified over 150 lice species from more than half of the bird species inhabiting the country (21).As Iran and Turkey share many bird species, it seems that many louse species remain to be discovered.Molecular phylogenetic analysis of avian lice from Iran will bring clearer understanding of the role of migratory birds in biogeographic distributions.
Names of orders are capitalized, and names of families are showed in bold.× The louse species is not normally found on this bird.Its report is probably due to contamination or misidentification.

FIGURE 9
FIGURE 9 Chewing lice identified in this study part VIII: (A-E) Colpocephalum heterosoma; (B) Head of large specimen ♂; (C) Head of small specimen, ♂; (D) Posterior end of small specimen ♂, and (E) Posterior end of small specimen ♀.

Table 1
Collected lice specimens belonged to 31 species from the families Philopteridae, Menoponidae, and Laemobothriidae.All of the identified lice species except C. aquilinus, L. vulturis, L. maximum, C. impressum, C. turbinatum, and C. heterographus are recorded for the first time from Iran ( ). Number of lice specimens collected from examined birds ranged from 1 to 55, the latter was a Bubo bubo Linnaeus, 1758.Mixed lice infestation was found in 11 birds, i.e., in one Philomachus pugnax (Linnaeus, 1758), two Himantopus himantopus Linnaeus, 1758, two Anas crecca Linnaeus, 1758, one Aquila nipalensis Hodgson, 1833, one Aquila rapax Temminck, 1828, two Gyps fulvus Hablitz, 1783, and two Strigiphilus sp.collected from Asio otus Linnaeus, 1758, one female Pectinopygus spp.collected from Anas clypeata Linnaeus, 1758 which is an unusual host and possibly was a contamination, one Laemobothrion spp.nymph, and four Quadraceps spp.(Figures Buteo buteo Linnaeus, 1758.Photomicrographs of examined lice specimens are presented in Figures2-14.Identification of few specimens could not be performed to species level including one damaged female

TABLE 1
Distribution of louse species of wild birds in some regions of Iran (September 2019 and December 2023) according to their host bird species.

TABLE 1 (
Continued) a according to International Union for Conservation of Nature (IUCN) Red List of Threatened Species (www.iucnredlist.org).Names of orders are capitalized, and names of families are showed in bold.

TABLE 2
Louse species reported from Iran according to their avian hosts until December 2023.