Study of Blood Parasites of the Three Snake Species in Iran: Natrix natrix, Natrix tessellata and Zamenis longissimus (Colubridae)

Document Type : Research Article

Authors

Department of Biology, Faculty of Science, University of Guilan, Rasht, Iran

Abstract

Infections with blood parasites are common phenomenon in reptiles from all over the world. Apicomplexan are the majority of blood parasites that frequently occur with high levels of parasitaemia in the snakes. The aim of this study was to determine the presence of blood parasites in some snakes Guilan province in the North of Iran. A total of 51 specimens of three snake species were captured including 18 specimens of Natrix natrix, 30 of Natrix tessellata and three from Zamenis longissimus. Blood sampling was carried out from the caudal vein by insulin syringe. The blood smears were stained with Giemsa solution and examined by light microscopy for heamoparasites. We found one species of Hepatozoon sp. as well as two intra-erythrocytic structures that we referred them to Rickettsia and Serpentoplasma in the snakes. The Serpentoplasmawith small amoeboid shape only detected in N. tessellate. But the Rickettsia which is bigger in size and formed roughly spherical inclusions detected in both Natrix species. This finding of haemoparasites represents for the first time in these snakes.

Keywords


Cook CA, Netherlands EC, Smit NJ. 2016. Redescription, molecular characterization and taxonomic re-evaluation of a unique African monitor lizard haemogregarine Karyolysus paradoxa (Dias, 1954) n. comb. (Karyolysidae). Parasites & Vectors 9: 347.
Davis JR, Boyle SA, Khana A, Gaya LJ, Grishamj M, Luque LE. 2012. Snake parasitism in an urban old-growth forest. Urban Ecosyst 15: 739-752.
Desser SS, Barta JR. 1984. An intraerythrocytic virus and Rickettsia of frogs from Algonquin Park, Ontario. J. Zool 62: 1521-1524.
Dvorakova N, Kvicerova J, Papousek I, Javanbakht H, Tiar G, Kami H, Siroky P. 2014. Haemogregarines from western Palaearctic freshwater turtles (genera Emys, Mauremys) are conspecific with Haemogregarina stepanowi Danilewsky, 1885. Parasitology 141: 522-530.
Han H, Wu Y, Dong H, Zhu S, Li L, Zhao Q, Wu D, Pei E, Wang Y, Huang B. 2015. First report of Hepatozoon (Apicomplexa: Adeleorina) from king ratsnakes (Elaphe carinata) in Shanghai, with description of a new species. Acta Parasitol 60(2): 266-274.
Jacobson E. 2007. Infectious diseases and pathology of reptiles, Pimera. Boca Ratón-USA.
Javanbakht H, Široký P, Mikulíček P, Sharifi M. 2015a. Distribution and abundance of Hemolivia mauritanica (Apicomplexa: Haemogregarinidae) and its vector Hyalomma aegyptiumin tortoises of Iran. Biologia 70(2): 229-234.
Javanbakht H, Kvicerova J, Dvorakova N, Mikulıcek P, Sharifi M, Kautmand M,  Marsıkova M, Siroky P. 2015b. Phylogeny, Diversity, Distribution, and Host Specificity of Haemoproteus spp. (Apicomplexa: Haemosporida: Haemoproteidae) of Palaearctic Tortoises. J. Eukaryot. Microbiol 62: 670-678.
Latifi M. 2000. The snakes of Iran. 3rd Edition. Department of Environment, Tehran, Iran.
Levine ND. 1988. The protozoan phylum Apicomplexa, Volume 1. CRC Press Inc., Boca Raton, Florida, pp 203.
Mebert K. 2011.The dice snake, Natrix tessellata: biology, distribution and conservation of a Palaearctic species. Mertensiella 18, DGHT, Rheinbach, Germany.
Morrison DA. 2009. Evolution of the Apicomplexa: Where are we now? Trends Parasitol 25: 375-382.
Nasiri V, Mobedi I, Dalimi A, Zare Mirakabadi A, Ghaffarifar F, Teymurzadeh S, Karimi G, Abdoli A, Paykari H. 2014. A description of parasites from Iranian snakes. Exp Parasitol 147: 7-15.
Patterson JW, Peirce MA. 1982. Intraerythrocytic parasites of reptiles from Lochinvar National Park, Zambia. Afr. J. Ecol 20: 293-295.
Peirce MA, Castleman ARW. 1974. An intraerythrocytic parasite of the Moroccan tortoise. J Wildl Dis 10: 139-142.
Peirce MA, Adlard RD. 2004. Haemoparasites from clinical screening of reptiles in south-east Queensland, Australia. Vet Rec 155: 708-709.
Pienaar UD. 1962. Haematology of some South African reptiles. Witwatersrand Univ. Pr, Johannesburg.
Rajabi F, Javanbakht H, Sajjadi SS. 2017. A preliminary study of haemoparasites in marsh frogs, Pelophylax ridibundus (Ranidae) from Iran. J Entomol Zool Stud 5(4): 1314-1317.
Sloboda M, Kamler M, Bulantova J, Votypka J, Modry D. 2007. A new species of Hepatozoon (Apicomplexa: Adeleorina) from Python regius (Serpentes: Pythonidae) and its experimental transmission by a mosquito vector. J Parasitol 93(5):1189-1198.
Sloboda M, Kamler M, Bulantová J, Votýpka J, Modrý D. 2008. Rodents as intermediate hosts of Hepatozoon ayorgbor (Apicomplexa: Adeleina: Hepatozoidae) from the African ball python, Python regius? Folia Parasitol 55: 13-16.
Smith TG. 1996. The genus Hepatozoon (Apicomplexa: Adeleina). J. Parasitol 82: 565-585.
Svahn k. 1974. Incidence of blood parasites of the genus Karyolysus (coccidia) in Scandinavian lizards. Oikos (kobenhavn) 25(1): 43-53.
Szczerbak NN. 2003. Guide to the reptiles of the eastern Palearctic. Florida: Krieger Publishing Company. pp 260.
Telford SR, Butler JF, Telford RS. 2002. Hepatozoonspecies (Apicomplexa: Hepatozoidae) of the corn snake, Elaphe guttata (Serpentes: Colubridae) and the pigmy rattlesnake, Sistrurus miliarius barbouri (Serpentes: Viperidae) in south Florida. J Parasitol 88: 778-782.
Telford SR, Ernst JA, Clark AM, Butler JF. 2004. Hepatozoon sauritus: A polytopic hemogregarine of three genera and four species of snakes in North Florida, with specific identity verified from genome analysis. J Parasitol 90: 352-358.
Telford SR. 2009. Hemoparasites of Reptilia, Color Atlas and Text. CRC Press, Taylor & Francis Group: Boca Raton, Florida, USA.
Ursula H, Rüdiger K, Mutschmann F, Rinder M. 2014. Blood parasites in reptiles imported to Germany. Parasitol Res 113(12): 4587-99.
Vaissi S, Parto P, Haghighi ZMS, Sharifi M. 2016. Intraerythrocytic rickettsial inclusions in endangered Kaiser’s mountain newt, Neurergus kaiseri (Caudata: Salamandridae). J Appl Anim Res 45: 1-3
Whiley H, Custance G, Graves G, Tenos J,Taylor M, Ross K, Gardner MG. 2016. Rickettsia Detected in the Reptile Tick Bothriocroton hydrosauri from the Lizard Tiliqua rugosa in South Australia. Pathogens 5, 41.