Parasites of reptiles in Iran (1922–2023): A literature review

Abstract

Reptiles are among the most diverse groups of animals, inhabiting nearly all continents and environments. Understanding their parasite biodiversity has garnered significant interest, particularly from a One Health perspective. Although the highly diverse reptile fauna of Iran, comprising 272 species i.e. 89 snakes (Serpentes), 171 lizards (Sauria), 8 turtles, 2 tortoises (Testudines), 1 crocodile (Crocodilia), and 1 worm-lizard (Amphisbaenia), there is a shortage of information about parasites. The present review is a compilation of 62 studies published from 1922 to August 2024. We present information on 56 species of reptiles from five groups (amphisbaenians, crocodiles, testudines, snakes, and lizards) and 98 parasitic taxa belonging to different protozoa and metazoa i.e. nematodes, cestodes, trematodes, acanthocephala, leeches, ticks, mites, and myiasis -producing flies. Although 63 taxa were diagnosed at the species level, 35 parasite taxa were only reported at the genus or family levels. Reviewing the literature, we found a paucity of information about endemic reptiles several of which are vulnerable species. Considering that some of the detected parasites e.g. Cryptosporidium and amoebae have serious clinical and/or public health threats molecular diagnostic techniques are needed for precise identification and understanding of the epidemiology and the potential zoonotic implications associated with parasites of reptiles. There is also a need to understand the exact distribution and host-parasite associations in different reptilian species present in Iran including the role of the reptiles as intermediate and reservoir hosts.

Graphical abstract

Highlights

• •The present review is a compilation of studies published from 1922 to August 2024.
• •We present parasites reported from 56 species of reptiles.
• •To date, 98 parasitic taxa belonging to different protozoa and metazoa have been reported.
• •We found a paucity of information about native reptiles many of which are vulnerable species.

1. Background

Reptiles are among the most diverse groups of animals that inhabit almost all continents and environments (Roll et al., 2017). This class of animals includes about 1200 genera, and more than 11,000 species mainly within four orders i.e. Squamata (lizards, snakes, and worm-lizards), Testudines (turtles and tortoises), Crocodylia (land and sea crocodiles) and Rhynchocephalia (i.e., one species of tuataras namely Sphenodon punctatus) (Uetz et al., 2019). Like other animal groups, reptiles are hosts of viral, bacterial, and parasitic pathogens, some of which are of zoonotic concern (Mendoza-Roldan et al., 2023a, Mendoza-Roldan et al., 2023b). Reptiles live in and around human habitats, they are used as important sources of food, medicines, and materials (e.g., the leather industry) in some parts of the world, and become increasingly common domestic pets (Mendoza-Roldan et al., 2020). Hence, understanding the biodiversity of their parasites has become of great interest among researchers, especially from a One Health perspective, since reptiles are host to a range of potentially zoonotic parasites of many different taxa i.e. Alaria (trematoda), Spirometra (cestoda), Anisakis, Eustrongylides, Angiostrongylus, Gnathostoma and Trichinella (nematoda), Armillifer (pentastomida), Ophionyssus natricis (acari), Trypanosoma, Sarcocystis, Cryptosporidium (protozoa) (Leung, 2024; Mendoza-Roldan et al., 2023).

Iranian reptiles are the largest group of vertebrates living in the country. According to the latest official reports, the reptile fauna of Iran comprised 272 species i.e. 89 snakes (Serpentes), 171 lizards (Sauria), 8 turtles, 2 tortoises (Testudines), 1 crocodile (Crocodilia), and 1 worm-lizard (Amphisbaenia) (Kasfash et al., 2020; Mozaffari et al., 2016; Safaei-Mahroo, 2019; Šmíd et al., 2014). However, as a result of the advancement of molecular methods, there are growing pieces of evidence regarding a wider diversity (Mozaffari et al., 2020). To date (September 12, 2024), 213 Iran reptile species have been recorded in the International Union for Conservation of Nature and Natural Resources (IUCN) Red List of Threatened Species (www.iucnredlist.org) out of which 2 are Critically Endangered (CE), 4 Endangered (EN), 9 Vulnerable (VU), and 9 Near Threatened (NT); several being endemic in the Country (e.g. Iranian Mountain Steppe Viper Vipera ebneri, Montivipera albicornuta, Montivipera latifii).

Since so far, most available studies on reptiles in Iran have focused on ecological investigations of hosts and conservational aspects rather than on the parasites (Kafash et al., 2020; Zare Khormizi et al., 2021), this study aimed to review the published research on parasites of reptiles in Iran from 1931 to August 2024.

2. Methods

We checked all available documents on each of the search terms which included a combination of Iran or Iranian (in Persian, English, and French) with each of the words “snake”, “lizard”, “turtle”, “tortoise”, “reptile” and generic names of the parasites of reptiles extracted from different sources e.g. “Flynn's Parasites of Laboratory Animals” (Mitchell, 2007), “parasites in pet reptiles” (Rataj et al., 2011) and “zoonotic parasites of reptiles: a crawling threat” (Mendoza-Roldan et al., 2020). The databases and search engines employed for the present literature review were PubMed (https://pubmed.ncbi.nlm.nih.gov/), Google Scholar (https://scholar.google.com/), Scientific Information Database of Iran (www.sid.ir), the collection of defended theses at all Iranian universities (https://irandoc.ac.ir/) and the collection of proceedings of Iranian scientific congresses on veterinary medicine, animal science and parasitology (https://civilica.com/). Databases were last visited on September 12, 2024.

In total, 62 documents, comprising 61 articles in peer-reviewed journals and one article presented at a national conference, were found and included. The literature was extracted from Google Scholar (n = 35), Pubmed (n = 35), and Civilica (n = 1). No defended thesis with a focus on parasites of reptiles was found. In regards to the language, two were written in Persian, four in French, and 56 in English.

Valid names of the reported scientific names (both parasites and reptiles) in older literature were obtained from updated resources i.e. http://www.reptile-database.org/and https://www.gbif.org/.

3. Results and discussion

3.1. Protozoan infections

3.1.1. Blood parasites

Infections with protozoan parasites of blood are very common in reptiles globally. Hemoparasites of reptiles are included in five groups of 1. Plasmodiids (Plasmodium, Haemocystidium, Saurocytozoon, Fallisia, Haemoproteus, Progarnia), 2. Hemogregarines (Haemogregarina, Hepatozoon, Hemolivia, Karyolyses), 3. Hemococcidia (Schellackia, Lainsonia, Lankestrella), 4. Kinetoplastids (Trypanosoma, Sauroleishmania), 5. Piroplasmids (Sauroplasma, Serpentoplasma) (Telford, 2009). Many of these hemoparasites are morphologically similar to related protozoa of other vertebrates. While most infections are asymptomatic, heavy infections may result in anaemia (Mitchell, 2007). Furthermore, filarial larvae (Nematoda), in addition to rickettsial, chlamydial, and viral parasites of blood cells have frequently been found in snakes, chelonians, and lizards (Telford, 2009; Ursula et al., 2014). Common to these parasites is that they need arthropods or leeches as vectors for their development or transmission (Mitchell, 2007). In Iran so far, Hepatozoon spp., Leishmania/Sauroleishmania spp., Serpentoplasma spp., Aegyptianella spp., Hemolivia mauritanica, and microfilariae of Oswaldofilaria chlamydosauri have been investigated in the blood of reptiles by light microscopy (Javanbakht et al., 2015b; Kazemi et al., 2004; Molavi et al., 2018; Sajjadi and Javanbakht, 2017). One study recorded intraerythrocytic haemoparasites without sequential data or genus designation (Nasiri et al., 2014). There is only one PCR-based study in which Haemoproteus anatolicum and Haemoproteus caucasica were identified in tortoises (Javanbakht et al., 2015a) (Table 1). There is little known about vectors of reptiles’ hemoparasites in Iran. So far in only one study the role of the hard tick Hyalomma aegyptium in the transmission of Hemolivia mauritanica has been shown (Javanbakht et al., 2015b).

Table 1.

Haemoparasites of reptiles reported from Iran.

Parasite	Host	Common name	Reference
Leishmania sp.	Paralaudakia caucasia (Eichwald, 1831). Reported as Agama caucasica	Caucasian agama	(Kazemi et al., 2004, 2004b; Nadim et al., 1968a; b; Rashti et al., 1971)
	Mesalina martini (Boulenger, 1897). Reported as Eremias guttulata	Martin's desert racer
	Heremites auratus Linnaeus, 1758. Reported as Mabuya aurata	Golden grass skink
	Trapelus agilis (Olivier, 1807). Reported as Agama agilis	Brilliant ground agama
	Phrynocephalus scutellatus (Olivier, 1807). Reported as Phrynocephalus seatellatua	Gray toad head agama
	Laudakia melanura Blyth, 1854. Reported as Agama melanura	Black agama
	Tenuidactylus caspius (Eichwald, 1831). Reported as Cyrtopodion caspius	Caspian bent-toed gecko
Leishmania gymnodactyli	Tenuidactylus caspius (Eichwald, 1831). Reported as Cyrtopodion caspius	Caspian bent-toed gecko	Seyedi Rashti et al. (1994)
Haemogregarina stepanowi Danilewsky, 1885	Mauremys capsica (Gmelin, 1774)	Caspian pond turtle	(Dvořáková et al., 2014; Javanbakht and Sharifi, 2014)
	Emys orbicularis (Linnaeus, 1758)	European pond turtle
Haemogregarina sp.	Mauremys capsica (Gmelin, 1774)	Caspian pond turtle	Rakhshandehroo et al. (2016)
Haemocystidium grahamiShortt (1922)	Laudakia nupta (De Filippi, 1843)	Large-scaled rock agama	Shortt (1922)
Haemocystidium phyllodactyliShortt (1922)	Asaccus elisae (Werner, 1895). Reported as Phyllodactylus elisae	Elisa's leaf-toed gecko	Shortt (1922)
Haemoproteus anatolicum Orkun and Guven 2013	Testudo hermanni Gmelin, 1789. Reported as Testudo graeca	Hermann's tortoise	(Javanbakht et al., 2015a)
Haemoproteus caucasica Krasilnikov, 1965	Testudo horsfieldii Gray, 1844	Central Asian tortoise	(Javanbakht et al., 2015a)
	Testudo hermanni Gmelin, 1789. Reported as Testudo graeca	Hermann's tortoise
Hemolivia mauritanica (Sergent and Sergent, 1904)	Testudo horsfieldii Gray, 1844	Central Asian tortoise	Javanbakht et al. (2015b)
	Testudo hermanni Gmelin, 1789. Reported as Testudo graeca	Hermann's tortoise
Rickettsia sp. (Probably Aegyptianella)	Natrix natrix (Linnaeus, 1758)	European grass snake	Sajjadi and Javanbakht (2017)
	Natrix tessellata (Laurenti, 1768)	Dice snake
Serpentoplasma sp.	Natrix tessellata (Laurenti, 1768)	Dice snake	Sajjadi and Javanbakht (2017)
Hepatozoon ophisauri (Tartakovskii, 1913)	Pseudopus apodus (Pallas, 1775)	European glass lizard	Zechmeisterová et al. (2021)
Hepatozoon colubrid (Börner, 1901)	Zamenis longissimus (Laurenti, 1768)	Aesculapian snake	Zechmeisterová et al. (2021)
Hepatozoon sp.	Macrovipera lebetinus subsp. Obtusa (Dwigubsky, 1832). Reported as Macrovipera lebetina obtuse	West-Asian blunt-nosed viper	Junsiri et al. (2024)
	Cerastes gasperettii Leviton and Anderson, 1967	Arabian horned viper	Rashnavadi (2012)
	Zamenis longissimus (Laurenti, 1768)	Aesculapian snake
Oswaldofilaria chlamydosauri (Breinl, 1913). Microfilariae. Reported as Oswaldofilaria chlamydosauri (Breinl, 1912)	Paralaudakia caucasia (Eichwald, 1831)	Caucasian agama	Molavi et al. (2018)
Karyolysus sp.	Darevskia chlorogaster (Boulenger, 1908)	Green Bellied lizard	Javanbakht et al. (2022)
Lankestrella sp.	Eremias persica Blanford, 1875	Persian race-runner	Javanbakht and Hajiyan (2024)
	Ophisops elegansMendoza-Roldan et al., 2021	Snake-eyed lizard
Schellackia sp.	Darevskia chlorogaster (Boulenger, 1809)	Greenbelly lizard	Zechmeisterová et al. (2021)
	Lacerta strigata (Eichwald, 1831)	Caspian green lizard
Intraerythrocytic haemoparasites	Pseudocerastes persicus (Duméril, Bibron & Duméril, 1854)	Persian horned viper	Nasiri et al. (2014)
	Macrovipera lebetinus subsp. Obtusa (Dwigubsky, 1832). Reported as Macrovipera lebetina subsp. Obtusa	West-Asian blunt-nosed viper
	Naja siamensis Laurenti, 1768. Reported as Naja oxiana	Central Asian cobra
	Dolichophis caspius (Gmelin, 1789). Reported as Coluber caspius	Caspian whipsnake

Leishmania gymnodactyli was detected in Sergentomyia sintoni (Seyedi Rashti et al., 1994). Furthermore, Sergentomyia clydei and Sergentomyia dentata have been recognized as vectors of lizard leishmaniasis (Yaghoobi-Ershadi, 2012). Snakes and lizards contribute to the distribution of several Leishmania species pathogenic for humans such as Leishmania tropica the causative agent of cutaneous leishmaniasis (CL) (Zhang et al., 2016). Although CL is widely distributed in 25 of 31 Iranian provinces with an annual incidence of 30.9 per 100,000 in the Iranian population (Holakouie-Naieni et al., 2017) the role of reptiles in the epidemiology of CL in the country warrants further investigations.

3.1.2. Gastrointestinal protozoa

Reptiles are hosts for various flagellates (e.g. Giardia spp., Hexamita spp., Trichomonas spp.), amoebae (e.g. Entamoeba invadens), coccidia (e.g. Eimeria spp., Isospora spp., Cryptosporidium spp., Blastocystis spp.) and ciliates (e.g. Balantidium spp., Nyctotheroides spp.) (Greiner, 2003; Mitchell, 2007). Infection with these parasites may cause enteritis, weight loss, regurgitation, colitis, gastritis, and death (Wilson and Carpenter, 1996). In Iran, gastrointestinal protozoan parasites were studied in two studies in which Eimeria spp., Isospora spp., Cryptosporidium spp., Balantidium spp., Nyctotheroides spp., Cyclospora spp., trichomonads, and amoebae were recorded (Arabkhazaeli et al., 2018; Nasiri et al., 2014) (Table 2). Among the reported protozoan parasites Cryptosporidium spp. Has a potential risk for human infections (Díaz et al., 2013; Mendoza-Roldan et al., 2020, 2023, 2024; Traversa et al., 2008).

Table 2.

Protozoan parasites of reptiles reported from Iran.

Parasite	Host	Common name	Reference
Toxoplasma gondii (Nicolle and Manceaux, 1908)	Naja oxiana (Eichwald, 1831)	Central Asian cobra	Nasiri et al. (2016)
	Pseudocerastes fieldi Schmidt, 1930. Reported as Pseudocerastes persicus fieldi	Field's horned viper
	Montivipera raddei (Boettger, 1890). Reported as Vipera albicornuta	Caucasus viper
	Gloydius intermedius (Strauch, 1868). Reported as Agkistrodon intermedius caucasicus	Caucasian pit viper
	Macrovipera lebetinus subsp. Obtusa (Dwigubsky, 1832). Reported as Vipera lebetina obtusa	West-Asian blunt-nosed viper
Neospora caninum Dubey et al., 1988	Snakes
	Pseudocerastes fieldi Schmidt, 1930. Reported as Pseudocerastes persicus fieldi	Field's horned viper	Nasiri and Jameie (2023)
	Naja oxiana (Eichwald, 1831)	Central Asian cobra	Nasiri and Jameie (2023)
	Montivipera raddei (Boettger, 1890). Reported as Vipera albicornuta	Caucasus viper	Nasiri and Jameie (2023)
Eimeria sp.	Snakes
	Montivipera raddei (Boettger, 1890)	Caucasus viper	Nasiri et al. (2014)
	Vipera eriwanensis subsp. Eriwanensis (Reuss, 1933). Reported as Vipera ursinii eriwanensis	Alburzi viper	Nasiri et al. (2014)
	Python molurus (Linnaeus, 1758)	Indian rock python	Arabkhazaeli et al. (2018)
	Lizards
	Pogona vitticeps (Ahl, 1926)	Central bearded dragon	Arabkhazaeli et al. (2018)
Blastocystis sp.	Snakes
	Macrovipera lebetinus subsp. Obtusa (Dwigubsky, 1832). Reported as Macrovipera lebetina subsp. Obtusa	West-Asian blunt-nosed viper	Nasiri et al. (2014)
Trichomonads	Snakes
	Eryx jaculus (Linnaeus, 1758)	Javelin sand boa	Arabkhazaeli et al. (2018)
	Lizards
	Iguana iguana (Linnaeus, 1758)	Common green iguana	Arabkhazaeli et al. (2018)
Cryptosporidium sp.	Snakes
	Echis carinatus subsp. Sochureki Stemmler, 1969	Phoorsa	Arabkhazaeli et al. (2018)
	Ophiophagus hannah (Cantor, 1836)	King cobra	Arabkhazaeli et al. (2018)
	Macrovipera lebetinus subsp. Obtusa (Dwigubsky, 1832). Reported as Macrovipera lebetina subsp. Obtusa	West-Asian blunt-nosed viper	Arabkhazaeli et al. (2018)
	Lizards
	Iguana iguana (Linnaeus, 1758)	Common green iguana	Arabkhazaeli et al. (2018)
	Tiliqua scincoides (White, 1790)	Bluetongued lizard	Arabkhazaeli et al. (2018)
	Pogona vitticeps (Ahl, 1926)	Central bearded dragon	Arabkhazaeli et al. (2018)
	Tortoises
	Testudo horsfieldii Gray, 1844	Central Asian tortoise	Arabkhazaeli et al. (2018)
Balantidium sp.	Lizards
	Iguana iguana (Linnaeus, 1758)	Common green iguana	Arabkhazaeli et al. (2018)
	Tortoises
	Testudo horsfieldii Gray, 1844	Central Asian tortoise	Arabkhazaeli et al. (2018)
Amoebae	Lizards
	Iguana iguana (Linnaeus, 1758)	Common green iguana	Arabkhazaeli et al. (2018)
	Eublepharis macularius (Blyth, 1854)	Leopard gecko	Arabkhazaeli et al. (2018)
	Tortoises
	Testudo horsfieldii Gray, 1844	Central Asian tortoise	Arabkhazaeli et al. (2018)
Cyclospora sp.	Lizards
	Tiliqua scincoides (White, 1790)	Bluetongued lizard	Arabkhazaeli et al. (2018)
Isospora sp.	Lizards
	Pogona vitticeps (Ahl, 1926)	Central bearded dragon	Arabkhazaeli et al. (2018)
	Turtles
	Trachemys scripta subsp. Elegans (Wied, 1838)	Pondslider	Arabkhazaeli et al. (2018)
Hexamita batrachorum Swezy, 1915	Snakes
	Pseudocerastes fieldi Schmidt, 1930	Field's horned viper	Nasiri et al. (2014)
	Naja oxiana (Eichwald, 1831)	Central Asian cobra	Nasiri et al. (2014)
	Montivipera raddei (Boettger, 1890)	Caucasus viper	Nasiri et al. (2014)
	Macrovipera lebetinus subsp. Obtusa (Dwigubsky, 1832). Reported as Macrovipera lebetina subsp. Obtusa	Levant viper	Nasiri et al. (2014)
	Vipera eriwanensis subsp. Eriwanensis (Reuss, 1933). Reported as Vipera ursinii eriwanensis	Alburzi viper	Nasiri et al. (2014)
	Gloydius intermedius (Strauch, 1868). Reported as Agkistrodon intermedius caucasicus	Caucasian pit viper	Nasiri et al. (2014)
Nyctotheroides sp.	Snakes
	Pseudocerastes fieldi Schmidt, 1930. Reported as Pseudocerastes persicus fieldi	Field's horned viper	Nasiri et al. (2014)

3.1.2.1. Toxoplasma gondii

In one study molecular analysis identified the presence of Toxoplasma gondii DNA in the brain of 55 individual snakes from five different species i.e. Pseudocerastes fieldi Schmidt, 1930, Naja siamensis Laurenti, 1768, Montivipera raddei (Boettger, 1890), Macrovipera lebetina subsp. Obtusa (Dwigubsky, 1832) and Gloydius intermedius (Strauch, 1868; Nasiri et al., 2016). Toxoplasma gondii is an obligate intercellular protozoan parasite that can infect a wide range of warm- and cold-blooded animals as well as humans (Długońska, 2017). Due to its exceptionally wide range of warm- and cold-blooded hosts, Toxoplasma gondii is one of the most successful zoonotic parasites on the earth (Djurković-Djaković et al., 2019). Considering that in two studies that detected DNA of the parasite in tissues of snakes (Nasiri et al., 2016) (Anah and Al-Mayali, 2018) isolation of viable parasites was not attempted, the role of the reptiles in the epidemiology of toxoplasmosis remains dubious.

3.2. Helminthoses

Reptiles have important roles as both definitive and intermediate hosts of helminths (Carbonara et al., 2023; Šlapeta et al., 2017). Nematodes are among the most common parasites identified in reptiles worldwide (Bower et al., 2019; Kuśmierek et al., 2020), including in Iran where several studies were done highlighting the species diversity, prevalence, and potential pathological effects of these parasites on their hosts. Investigations on this topic date back to 1966 when Petter (1966) provided data about nematode taxonomy in reptiles. In 2004, nematodes of the European pond turtle were mentioned as part of a larger study investigating the pond culture of sturgeon (Pazooki and Aghaeei Moghadam, 2004). In further years, several studies were performed either specifically on reptiles or as part of a larger study that investigated nematodes of snakes, including venomous ones and lizards (Table 3). Nematode infection in Iranian reptiles indicates significant prevalence and a wide diversity of species, some of which e.g. Anisakis and Ophidascaris are likely to pose a considerable health risk to hosts (Hossain et al., 2023; Magnino et al., 2009).

Table 3.

Helminths of reptiles reported from Iran.

Parasite	Host species	Common name	Reference
Trematoda
Telorchis assula (Dujardin, 1845)	Natrix natrix (Linnaeus, 1758)	European grass snake	(Halajian et al., 2013; Nasiri et al., 2014; Shayegh et al., 2016; Yossefi et al., 2014; Yousesfi et al., 2013)
	Natrix tessellata (Laurenti, 1768)	Dice snake
	Emys orbicularis (Linnaeus, 1758)	European pond turtle
	Mauremys caspica (Gmelin, 1774)	Caspian turtle
Telorchis sp.	Mauremys caspica (Gmelin, 1774)	Caspian turtle	Youssefi et al. (2016)
Cestoda
Ophiotaenia europaea Odening, 1963	Natrix natrix (Linnaeus, 1758)	European grass snake	(Halajian et al., 2013; Yossefi et al., 2014; Youssefi et al., 2010)
	Natrix tessellata (Laurenti, 1768)	Dice Snake
Ophiotaenia sp.	Natrix natrix (Linnaeus, 1758)	European grass snake	Nasiri et al. (2014)
Oochoristica fibrata Meggitt, 1927	Boiga trigonata subsp. melanocephala (Annandale, 1904)	Indian gamma snake	Mariaux et al. (2017)
Oochoristica tuberculata (Rudolphi, 1819)	Varanus griseus (Daudin, 1803)	Desert monitor	(Dollfus, 1965; Goldberg and Bursey, 2010)
	Ophisops elegansMendoza-Roldan et al., 2021	Snake-eyed lizard
Oochoristica sp.	Platyceps rhodorachis (Jan 1865). Reported as Zamenis rhodorhachis	Aesculapian snake	Dollfus (1965)
	Malpolon monspessulanus subsp. insignitus	Montpellier snake
Nematotaenia dispar (Goeze, 1782)	Varanus griseus (Daudin, 1803)	Desert monitor	Dollfus (1965)
Nematotaenia sp.	Varanus griseus (Daudin, 1803)	Desert monitor	Dollfus (1965)
Joyeuxiella echinorhynchoides (Sonsino, 1884) cysticercoid	Platyceps najadum (Eichwald, 1831). Reported as Coluber najadum	Dahl's whip snake	Dollfus (1965)
Nematoda
Entomelas entomelas (Dujardin, 1845)	Pseudopus apodus (Pallas, 1775)	European glass lizard	Halajian et al. (2013)
Rhabdias fuscovenosa (Railliet, 1899)	Natrix natrix (Linnaeus, 1758)	European grass snake	(Halajian et al., 2013; Yossefi et al., 2014)
	Natrix tessellata (Laurenti, 1768)	Dice snake
Ascarididae	Naja oxiana (Eichwald, 1831)	Central Asian cobra	Nasiri et al. (2014)
Kalicephalus viperae (Rudolphi, 1819)	Macrovipera lebetinus (Linnaeus, 1758)	Levantine viper	Larki et al. (2023)
Abbreviata kazachstanicaMariaux et al., 2017	Pseudopus apodus (Pallas, 1775)	European glass lizard	Ghanbari Johkool et al. (2021)
Ophidascaris filaria (Dujardin, 1845)	Python molurus (Linnaeus, 1758)	Indian python	Ganjali et al. (2015)
Skrjabinodon pigmentatus (Mariaux et al., 2017)	Laudakia caucasia (Eichwald, 1831)	Caucasian agama	Rezazadeh et al. (2012)
Spauligodon lacertae Sharpilo, 1966	Laudakia caucasia (Eichwald, 1831)	Caucasian agama	Rezazadeh et al. (2012)
Thelandros baylisi (Chabaud, 1953)	Laudakia caucasia (Eichwald, 1831)	Caucasian agama	Rezazadeh et al. (2012)
Abbreviata baltazardi (Chabaud 1953)	Phrynocephalus helioscopus (Pallas, 1771)	Sunwatcher toadhead agama	Chabaud (1953)
Oswaldofilaria chlamydosauri (Breinl, 1913). Reported as Oswaldofilaria chlamydosauri (Breinl, 1912) microfilariae	Paralaudakia caucasia (Eichwald, 1831)	Caucasian agama	Molavi et al. (2018)
Thelandros agama Adamson and Nasher, 1984	Laudakia nupta (De Filippi, 1843)	Large-scaled rock agama	Rahimian et al. (2014)
Thelandros popovi (Mariaux et al., 2017)	Laudakia nupta (De Filippi, 1843)	Large-scaled rock agama	Rahimian et al. (2014)
Thelandros karkasensisRahimian et al., 2014	Laudakia nupta (De Filippi, 1843)	Large-scaled rock agama	Rahimian et al. (2014)
Thubunea sp.	Laudakia nupta (De Filippi, 1843)	Large-scaled rock agama	Rahimian et al. (2014)
Parapharyngodon thuliniRahimian et al., 2014	Laudakia nupta (De Filippi, 1843)	Large-scaled rock agama	Rahimian et al. (2014)
Alaeuris numidica (Seurat, 1918)	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
Mehdiella microstoma (Drasche, 1884)	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Mehdiella longissimi Petter (1966)	Testudo horsfieldii Gray, 1844	Central Asia tortoise	Petter (1966)
Mehdiella stylosa Thapar, 1925	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Mehdiella uncinata Drasche, 1884	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Tachygonetria conica (Drasche, 1884)	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Tachygonetria dentata (Drasche, 1884)	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Tachygonetria longicollis (Schneider, 1866)	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Tachygonetria palearcticus Seurat, 1918	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Tachygonetria pusilla Seurat, 1918	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Tachygonetria robusta (Drasche, 1884)	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Thaparia thapari (Dubinina, 1949)	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Atractis baltazardi Petter (1966)	Testudo graeca zarudnyi Nikolsky, 1896	Iranian tortoise	Petter (1966)
Falcaustra araxiana Massino, 1924	Emys orbicularis (Linnaeus, 1758)	European pond turtle	(Rajabloo et al., 2017; Shayegh et al., 2016)
Serpinema microcephalus (Dujardin, 1845)	Emys orbicularis (Linnaeus, 1758)	European pond turtle	(Hoseini et al., 2015; Shayegh et al., 2016; Youssefi et al., 2016)
	Mauremys caspica (Gmelin, 1774)	Caspian turtle
Falcaustra armenica Massino, 1924	Mauremys caspica (Gmelin, 1774)	Caspian turtle	Youssefi et al. (2016)
Oxyuridae	Mauremys caspica (Gmelin, 1774)	Caspian turtle	Youssefi et al. (2016)
Hysterothylacium sp.	Emys orbicularis (Linnaeus, 1758)	European pond turtle	Pazooki and Aghaeei Moghadam (2004)
Camallanus sp.	Emys orbicularis (Linnaeus, 1758)	European pond turtle	Pazooki and Aghaeei Moghadam (2004)
Anisakis sp.	Emys orbicularis (Linnaeus, 1758)	European pond turtle	Pazooki and Aghaeei Moghadam (2004)
Falcaustra ararath (Massino, 1924)	Mauremys caspica (Gmelin, 1774)	Caspian turtle	Rakhshandehroo et al. (2020)
Spiroxys sp.	Mauremys caspica (Gmelin, 1774)	Caspian turtle	Rakhshandehroo et al. (2020)
Strongylid egg	Iguana iguana (Linnaeus, 1758)	Common green iguana	Arabkhazaeli et al. (2018)
	Trapelus agilis (Olivier, 1807)	Brilliant ground agama
	Pogona vitticeps (Ahl, 1926)	Central bearded dragon
	Coluber nummifer Reuss, 1834	Asian racer
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
Oxyurid egg	Iguana iguana (Linnaeus, 1758)	Common green iguana	(Arabkhazaeli et al., 2018; Youssefi et al., 2016)
	Eublepharis macularius (Blyth, 1854)	Common leopard gecko
	Lacerta media Lantz and Cyrén, 1920	Medium lizard
	Pogona vitticeps (Ahl, 1926)	Central bearded dragon
	Macrovipera lebetinus subsp. Obtusa (Dwigubsky, 1832). Reported as Macrovipera lebetina subsp. Obtusa	Levant viper
	Testudo horsfieldii Gray, 1844	Central Asia tortoise
	Mauremys caspica (Gmelin, 1774)	Caspian terrapin
Strongyloides egg	Tiliqua scincoides (White, 1790)	Common bluetongue	(Arabkhazaeli et al., 2018; Nasiri et al., 2014)
	Macrovipera lebetinus subsp. Obtusa (Dwigubsky, 1832). Reported as Macrovipera lebetina subsp. Obtusa	Levant viper
	Ophiophagus hannah (Cantor, 1836)	Hamadryad
	Naja oxiana (Eichwald, 1831)	Central Asian cobra
	Vipera eriwanensis subsp. Eriwanensis (Reuss, 1933). Reported as Vipera ursinii eriwanensis	Alburzi viper
Acanthocephala
Centrorhynchus corvi Fukui, 1929	Naja oxiana (Eichwald, 1831)	Central Asian cobra	Nasiri et al. (2014)
	Montivipera raddei (Boettger, 1890)	Caucasus viper
	Macrovipera lebetinus subsp. Obtusa (Dwigubsky, 1832). Reported as Macrovipera lebetina subsp. Obtusa	West-Asian blunt-nosed viper
	Coluber caspius Gmelin in Linnaeus, 1789	European whip snake
Leech
Haementeria costata (Müller, 1846). Also reported as Placobdella costata	Emys orbicularis (Linnaeus, 1758)	European pond turtle	(Hojjati et al., 2003; Kami et al., 2006)

Cestodes, on the other hand, can infect various reptiles with different pathological effects on the affected animals. In Iran, the European grass snakes (Natrix natrix) as well as the European glass lizard (Pseudopus apodus) are hosts for Ophiotaenia spp. (Nasiri et al., 2014). The first mention of cestodes in Iranian reptiles dates back to 1965 (Dollfus, 1965) with a publication that provided some detailed descriptions and classifications of various cestode species (Table 3). More recently, Mariaux et al. (2017) investigated the cestode diversity of reptiles with a highlight on the need for improved taxonomic and molecular approaches for the identification of different cestode species.

Trematodes are common helminths of reptiles with many species being reported at a global level (Bower et al., 2019). However, in Iran, few studies investigated the infection of reptiles by trematodes, and they include only snakes and turtles as investigated hosts (Halajian et al., 2013; Nasiri et al., 2014; Shayegh et al., 2016; Yossefi et al., 2014; Yousesfi et al., 2013, 2016). A total of 87 individual grass snakes (Natrix natrix) and dice snakes (Natrix tessellata) were investigated in three studies in Iran and an important proportion of them was infected by Telorchis assula (Halajian et al., 2013; Nasiri et al., 2014b; Yossefi et al., 2014), underlying the lack of data on this topic. The same trematode species, Telorchis assula was identified in the European pond turtle (Emys orbicularis) from Fars province with a high prevalence (48.07%) (Shayegh et al., 2016) suggesting a potential role as reservoir hosts for other reptiles. Additionally, the Caspian turtle (Mauremys caspica) was also found infected by Telorchis spp. (Youssefi et al., 2016). Although several trematodes are known to infect reptiles (Hughes et al., 1942), only Telorchis assula was reported in Iranian reptiles highlighting the need for further research to understand the real diversity of species as well as the impact of these infections on reptilian health.

Finally, acanthocephalans, generally known as thorny-headed helminths, can infect various hosts, including reptiles (Smales, 2014), and have severe health implications, like malnutrition and even death (Nasiri et al., 2014). In Iran, few studies have investigated the occurrence of acanthocephalans in local reptiles (Table 3). In snakes, larval stages of Centrorhynchus corvi were identified in the intestinal wall of seven snakes, associated with local necrosis (Nasiri et al., 2014b).

3.3. Ectoparasites

Parasitic arthropods of reptiles are important due to their role as parasites, but mainly because of their vectorial competence for various diseases (Mendoza-Roldan et al., 2021). In Iran, ticks and mites were mainly investigated in reptiles (Table 4). The first knowledge in Iran about ectoparasites in reptiles was documented (Baltazard et al., 1955; Vercammen-Grandjean et al., 1970) which identified several mite and tick species and provided some information on this topic.

Table 4.

Ectoparasites of reptiles reported from Iran.

Parasite	Host species	Common name	Reference
Ticks
Ornithodoros tartakovskyi Olenev, 1931	Testudine (French word: tortues)		Baltazard et al. (1955)
Ornithodoros erraticus Clifford, Kohls & Sonenshine, 1964	Testudine (French word: tortues)		Baltazard et al. (1955)
Hyalomma aegyptium Linnaeus, 1758	Testudo sp.	NS	(Abbassian-Lintzen, 1960; Banafshi et al., 2018)
	Lizard	NS	Abbassian-Lintzen (1960)
	Testudo graeca Linnaeus, 1758	Mediterranean spur-thighed tortoise	(Adeli-Sardou et al., 2019; Banafshi et al., 2018; Javanbakht et al., 2015b; Nabian and Mirsalimi, 2002; Razmjo et al., 2013; Tavassoli et al., 2007)
	Laudakia nupta (De Filippi, 1843)	Large-scaled rock agama	Razmjo et al. (2013)
	Trachylepis vittata (Olivier, 1804)	Bridled mabuya	Razmjo et al. (2013)
	Heremites auratus Linnaeus, 1758. Reported as Trachylepis aurata subsp. transcaucasica	Golden grass skink	Razmjo et al. (2013)
	Trapelus ruderatus (Olivier, 1804) (Trapelus lessonae)	Anderson's agama	Razmjo et al. (2013)
	Testudo horsfieldii Gray, 1844	Central Asian tortoise	Javanbakht et al. (2015b)
Haemaphysalis sp.	Trachylepis vittata (Olivier, 1804)	Bridled mabuya	Razmjo et al. (2013)
	Heremites auratus Linnaeus, 1758. Reported as Trachylepis aurata subsp. transcaucasica	Golden grass skink	Razmjo et al. (2013)
	Trapelus ruderatus (Olivier, 1804) (Trapelus lessonae)	Anderson's agama	Razmjo et al. (2013)
	Laudakia nupta (De Filippi, 1843)	Large-scaled rock agama	Razmjo et al. (2013)
Rhipicephalus sanguineus sensu lato Latreille, 1806	Trachylepis vittata (Olivier, 1804)	Bridled mabuya	Razmjo et al. (2013)
	Heremites auratus Linnaeus, 1758. Reported as Trachylepis aurata subsp. transcaucasica	Golden grass skink	Razmjo et al. (2013)
	Trapelus ruderatus (Olivier, 1804) (Trapelus lessonae)	Anderson's agama	Razmjo et al. (2013)
	Laudakia nupta (De Filippi, 1843)	Large-scaled rock agama	Razmjo et al. (2013)
Hyalomma marginatum Koch, 1844. Reported as Hyalomma marginatum subsp. marginatum	Testudo graeca Linnaeus, 1758	Mediterranean spur-thighed tortoise	Adeli-Sardou et al. (2019)
Hyalomma rufipes Koch, 1844. Reported as Hyalomma marginatum subsp. rufipes	Testudo graeca Linnaeus, 1758	Mediterranean spur -thighed tortoise	Adeli-Sardou et al. (2019)
Mite
Hexidionis agamae Andre, 1929	Agama sp.	Agamas	Vercammen-Grandjean et al. (1970)
Ophionyssus natricis (Geravis, 1844)	Python bivittatus (Kuhl, 1820)	Burmese python	Amanatfard et al. (2014)
Geckobiella donnae Paredes-León, Klompen & Pérez, 2012	Iguana iguana (Linnaeus, 1758)	Common green iguana	Sharifzadeh et al. (2016)
Hirstiella sp.	Iguana iguana (Linnaeus, 1758)	Common green iguana	Tavassoli et al. (2017)
Schoengastia sp.	Lacerta strigata Eichwald, 1831	Caspian green lizard	(Mariaux et al., 2017)
Pentidionis agamae (André, 1929)	Agama sp.		Vercammen-Grandjean et al. (1970)
Miyasis
Calliphora vicina Robineau-Desvoidy, 1830	Testudo graeca Linnaeus, 1758	Mediterranean spur-thighed tortoise	Ahmadiara et al. (2011)
Musca domestica Linnaeus, 1758	Pseudocerastes persicus (Duméril, Bibron & Duméril, 1854)	Persian horned viper	Dehghani et al. (2012)

∗NS: not stated.

The impact of ticks on reptile health was documented by Abbassian-Lintzen (1960) and Razmjo et al. (2013) who associated the infestation by mites and ticks with anaemia, skin disorders, and transmission of pathogens. Later on, Amanatfard et al. (2014) described a case of dermatitis caused by mite infestation in a reptile owner. More recently, epidemiological studies focused on the distribution of mites in various regions in Iran were done, including correlations of infestation with environmental factors (Orlova et al., 2023; Tavassoli et al., 2017). Myiasis was also reported in snakes (Dehghani et al., 2012) and in Testudo graeca (Ahmadiara et al., 2011) in Iran, pointing out the need for early diagnosis and treatment for the protection of reptilian fauna (Table 4).

4. Conclusions

This paper offers a comprehensive literature review of parasites in reptiles from Iran, with data collected from 1931 to August 2024. Constant parasite survey in endemic reptiles is important considering several species are of conservation concern. It is worth noting that the exact distribution and host-parasite associations should be known and more studies are needed with a focus on new study areas and different reptile species. Advanced diagnosis techniques are needed for accurate identification as well as for understanding the epidemiology and the potential zoonotic implications. Strategies for reptile health, species conservation, and the One Health implications should be developed. Considering the risk of co-endangerment and co-extinction of the parasites and their hosts (Gómez and Nichols, 2013), the conservation of parasites of reptiles in Iran especially those infecting endangered hosts should be thought of as a critical mission.

CRediT authorship contribution statement

Alireza Sazmand: Writing – review & editing, Writing – original draft, Validation, Supervision, Project administration, Methodology, Investigation, Conceptualization. MohammadParsa Miadfar: Writing – original draft, Methodology. Georgiana Deak: Writing – original draft, Methodology. Mohammad Babaei: Writing – original draft, Methodology. Jairo A. Mendoza-Roldan: Writing – review & editing. Domenico Otranto: Writing – review & editing.

Declaration of competing interest

The authors declare no conflict of interest.