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Morphological and molecular characterisation of Haemogregarina sp. (Apicomplexa: Adeleina: Haemogregarinidae) from the blood of the Caspian freshwater turtle Mauremys caspica (Gmelin) (Geoemydidae) in Iran


To date, a number of species of Haemogregarina have been described from different turtle hosts, mainly based on the morphology of the developmental stages detected in the host erythrocytes. The diversity and overlapping morphological features in the old and recent descriptions has led to considerable complications in the taxonomy of Haemogregarina spp. In this study, different stages of maturity and developing gamonts of a putative new species of Haemogregarina were detected in erythrocytes of the Caspian turtle Mauremys caspica (Gmelin) (Geoemydidae) originating from a southern province in Iran. Although some of the morphological characteristics were consistent with Haemogregarina stepanowi Danilewsky, 1885, some new observations were made, particularly in the gamont stage. The phylogenetic analysis based on 18S rDNA sequences revealed that the present isolate appears as basal to a large clade of Haemogregarina spp. with sequences available in the GenBank database. In accordance with the phylogenetic results, the present Iranian isolate showed a higher degree of interspecific divergence (up to 3.3%) compared to the data for the taxa available in the GenBank database. Thus, molecular data indicate that this isolate may represent a new species. However, further genetic analyses are needed as a complementary tool to the morphological characterisation in order to elucidate the phylogenetic relationships of Haemogregarina spp.

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  1. Billet, M. A. (1904). A propos de l’Hémogrégarine de émyde lépreuse (Emys leprosa Schw) de l’Afrique du Nord. Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie. Paris, 56, 482–484.

  2. Campbell, T. W., & Ellis, C. K. (2007). Avian and exotic animal hematology and cytology. Ames, IA: Blackwell Publishing.

  3. Danilewsky, B. (1885). Die Hämatozoën der Kaltblüter. Archiv für Mikroskopische Anatomie, 24, 588–598.

  4. Davies, A. J., & Johnston, M. R. L. (2000). The biology of some intraerythrocytic parasites of fishes, amphibians and reptiles. Advances in Parasitology, 45, 1–107.

  5. Davis, A. K., & Sterrett, S. C. (2011). Prevalence of haemogregarine parasites in three freshwater turtle species in a population in Northeast Georgia, USA. International Journal of Zoology Research, 7, 156–163.

  6. De Campos Brites, V. L., & Rantin, F. T. (2004). The influence of agricultural and urban contamination on leech infestation of freshwater turtles, Phrynops geoffroanus, taken from two areas of the Uberabinha River. Environmental Monitoring and Assessment, 96, 273–281.

  7. Ducloux, M. L. (1904). Sur une Hemogregarine de Emys leprosa. Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie, Paris, 56, 564–565.

  8. Dvořáková, N., Kvicerova, J., Papousek, I., Javanbakht, H., Tiar, G., Kami, H. G., & Siroky, P. (2014). Haemogregarines from western Palaearctic freshwater turtles (genera Emys, Mauremys) are conspecific with Haemogregarina stepanowi Danilewsky, 1885. Parasitology, 14, 522–530.

  9. Dvořáková, N., Kvicerova, J., Hostovsky, M., & Siroky, P. (2015). Haemogregarines of freshwater turtles from Southeast Asia with a description of Haemogregarina sacaliae sp. n. and a redescription of Haemogregarina pellegrini Laveran and Pettit. Parasitology, 142, 816–826.

  10. Jakes, K. A., Donoghue, P. J., & Cameron, S. L. (2003). Phylogenetic relationships of Hepatozoon (Haemogregarina) boigae, Hepatozoon sp., Haemogregarina clelandi and Haemoproteus chelodina from Australian reptiles to other Apicomplexa based on cladistic analyses of ultrastructural and life-cycle characters. Parasitology, 126, 555–559.

  11. Javanbakht, H., & Sharifi, M. (2014). Prevalence and intensity of Haemogregarina stepanowi (Apicomplexa: Haemogregarinidae) in two species of freshwater turtles (Mauremys caspica and Emys orbicularis) in Iran. Journal of Entomology and Zoology Studies, 2, 155–158.

  12. Kopecná, J., Jirků, M., Oborník, M., Tokarev, Y. S., Lukes, J., & Modrý, D. (2006). Phylogenetic analysis of coccidian parasites from invertebrates: Search for missing links. Protist, 157, 173–183.

  13. Laveran, A., & Pettit, A. (1909). Contribution à l’étude des hémogrégarines de Clemmys leprosa et de Chelodina longicollis. Bulletin de la Société de Pathologie Exotique, 2, 377–380.

  14. Levine, N. D. (1988). The protozoan phylum Apicomplexa (Vol. II). Boca Raton, Florida: CRC Press., 224 pp

  15. Lv, Z., Wu, Z., Zhang, L., Ji, P., Cai, Y., Lou, S., et al. (2015). Genome mining offers a new starting point for parasitology research. Parasitology Research, 114, 399–409.

  16. Mihalca, A., Racka, K., Gherman, C., & Ionescu, D. T. (2008). Prevalence and intensity of blood apicomplexan infections in reptiles from Romania. Parasitology Research, 102, 1081–1083.

  17. Paperna, I. (1989). Developmental cycle of chelonian hemogregarines in leeches with extraintestinal multiple sporozoite oocysts and a note on the blood stages in the chelonian hosts. Diseases of Aquatic Organisms, 7, 149–153.

  18. Paterson, W. B., & Desser, S. S. (1976). Observations on Haemogregarina balli sp. n. from the common snapping turtle, Chelydra serpentina. Journal of Protozoology, 23, 294–301.

  19. Petit, G., Landau, I., Baccam, D., & Lainson, R. (1990). Descriptionet cycle biologique d’Hemolivia stellata n. g., n. sp., hémogrégarine de crapauds Brésiliens. Annales de Parasitologie Humaine et Comparée, 65, 3–15.

  20. Reichenow, E. (1910). Haemogregarina stepanowi. Die Entwicklungsgeschichte einer Hamogregarine. Archiv für Protistenkunde, 20, 251–350.

  21. Siddall, M. E., & Desser, S. S. (1990). Gametogenesis and sporogonic development of Haemogregarina balli (Apicomplexa: Adeleina: Haemogregarinidae) in the leech Placobdella ornata. Journal of Protozoology, 37, 511–520.

  22. Siddall, M. E., & Desser, S. S. (1992). Prevalence and intensity of Haemogregarina balli (Apicomplexa: Adeleina: Haemogregarinidae) in three turtle species from Ontario, with observations on intraerythrocytic development. Canadian Journal of Zoology, 70, 123–128.

  23. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

  24. Telford, S. R. (2009). Hemoparasites of the Reptilia: Color Atlas and Text. Boca Raton: CRC Press, pp. 245–252.

  25. Xiao, L., Escalante, L., Yang, C., Sulaiman, I., Escalante, A. A., Montali, R. J., et al. (1999). Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Applied and Environmental Microbiology, 65, 1578–1583.

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Financial support

This work was financially supported by a research grant from Shiraz University, Shiraz, Iran (Grant No. 94-GR-VT-5).

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Correspondence to Ehsan Rakhshandehroo.

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All applicable institutional, national and international guidelines for the care and use of animals were followed.

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Rakhshandehroo, E., Sharifiyazdi, H. & Ahmadi, A. Morphological and molecular characterisation of Haemogregarina sp. (Apicomplexa: Adeleina: Haemogregarinidae) from the blood of the Caspian freshwater turtle Mauremys caspica (Gmelin) (Geoemydidae) in Iran. Syst Parasitol 93, 517–524 (2016).

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