Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-23T09:34:47.363Z Has data issue: false hasContentIssue false
  • English
  • Français

Haemogregarines from western Palaearctic freshwater turtles (genera Emys, Mauremys) are conspecific with Haemogregarina stepanowi Danilewsky, 1885

Published online by Cambridge University Press:  26 November 2013

NELA DVOŘÁKOVÁ ,
JANA KVIČEROVÁ ,
IVO PAPOUŠEK ,
HOSSEIN JAVANBAKHT ,
GHOULEM TIAR ,
HAJIGHOLI KAMI  and
PAVEL ŠIROKÝ
NELA DVOŘÁKOVÁ
Affiliation:
Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1/3, 612 42 Brno, Czech Republic CEITEC-Central European Institute of Technology, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1/3, 612 42 Brno, Czech Republic
JANA KVIČEROVÁ
Affiliation:
Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic Department of Parasitology, Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
IVO PAPOUŠEK
Affiliation:
Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1/3, 612 42 Brno, Czech Republic
HOSSEIN JAVANBAKHT
Affiliation:
Department of Biology, Razi University, Baghabrisham 67149, Kermanshah, Iran
GHOULEM TIAR
Affiliation:
Department of Biology, University of Badji Mokhtar, BP 12, El Hadjar, 23000 Annaba, Algeria
HAJIGHOLI KAMI
Affiliation:
Department of Biology, Faculty of Science, Golestan University, Gorgan, Iran
PAVEL ŠIROKÝ*
Affiliation:
Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1/3, 612 42 Brno, Czech Republic CEITEC-Central European Institute of Technology, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1/3, 612 42 Brno, Czech Republic
*
*Corresponding author: Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1/3, 612 42 Brno, Czech Republic. E-mail: sirokyp@vfu.cz
Get access Rights & Permissions [Opens in a new window]

Summary

The majority of Haemogregarina species have been based on the morphology of their erythrocytic stages and supposed strict host specificity. The quantity of species with a limited number of overlapping diagnostic traits has led to a considerable mess in haemogregarine taxonomy and significant synonymy. We analysed host specificity, intra- and interspecific variability, evolutionary relationships, and the distribution of the type species of the genus Haemogregarina – H. stepanowi. The morphology of blood stages and 18S rDNA sequences of this haemogregarine from four western Palaearctic hard-shelled freshwater turtles (Emys orbicularis, Mauremys caspica, Mauremys leprosa and Mauremys rivulata) were compared with Haemogregarina balli. Additional sequences of 18S rDNA of Haemogregarina-like isolates collected from three species of African hinged terrapins (genus Pelusios) were used to enlarge the dataset for phylogenetic analyses. Thirteen sequences (1085 bp) of Haemogregarina representing all four western Palaearctic turtle species were identical, corresponding to H. stepanowi, which is closely related to the Nearctic species H. balli. In our analyses, Haemogregarina spp. constituted a monophyletic clade sister to the genus Hepatozoon. Haemogregarina stepanowi possesses a wide distribution range from the Maghreb, through Europe, Turkey and the Middle East to Iran. We consider that the genus Haemogregarina has a low host specificity crossing the family level of its vertebrate hosts and that its distribution is likely to be linked to the vector and definitive host – the leech.

Keywords

ApicomplexaHaemogregarinaEmysMauremysPelusios18S rDNAphylogenetic analysishost specificity
Type
Research Article
Information
Parasitology , Volume 141 , Issue 4 , April 2014 , pp. 522 - 530
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Barta, J. R. (1989). Phylogenetic analysis of the class Sporozoea (phylum Apicomplexa Levine, 1970): evidence for independent evolution of heteroxenous life cycles. Journal of Parasitology 75, 198–206.CrossRefGoogle ScholarPubMed
Barta, J. R., Ogedengbe, J. D., Martin, D. S. and Smith, T. G. (2012). Phylogenetic position of the adeleorinid coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) inferred using 18S rDNA sequences. Journal of Eukaryotic Microbiology 59, 171–180.Google Scholar
Bielecki, A., Cichocka, J. M., Jabłoński, A., Jeleń, I., Ropelewska, E., Biedunkiewicz, A., Terlecki, J., Nowakowski, J. J., Pakulnicka, J. and Szlachciak, J. (2012). Coexistence of Placobdella costata (Fr. Müller, 1846) (Hirudinida: Glossiphoniidae) and mud turtle Emys orbicularis . Biologia 67, 731–738.CrossRefGoogle Scholar
Billet, M. A. (1904). A propos de l'Hémogrégarine de l'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.Google Scholar
Brumpt, E. (1904). Contribution á l'étude d'évolution des hémogrégarines et des trypanosomes. Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie. Paris 57, 165–167.Google Scholar
Carreno, R. A., Martin, D. S. and Barta, J. R. (1999). Cryptosporidium is more closely related to the gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small-subunit ribosomal RNA gene sequences. Parasitology Research 85, 899–904.Google Scholar
Criado-Fornelio, A., Ruas, J. L., Casado, N., Farias, N. A., Soares, M. P., Muller, G., Brumt, J. G., Berne, M. E., Buling-Sarana, A. and Barba-Carretero, J. C. (2006). New molecular data on mammalian Hepatozoon species (Apicomplexa: Adeleorina) from Brazil and Spain. International Journal for Parasitology 92, 93–99.Google Scholar
Danilewsky, B. (1885). Die Hämatozoën der Kaltblüter. Archiv für Mikroskopische Anatomie 24, 588–598. +Taf. XXVIIA.CrossRefGoogle Scholar
Desser, S. S. (1993). The Haemogregarinidae and Lankesterellidae. In Parasitic Protozoa, Vol. 4, 2nd Edn. (ed. Kreier, J. P.), pp. 247–272. Academic Press, New York, NY, USA.Google Scholar
Desser, S. S. and Yekutiel, D. (1987). Blood parasites of amphibians and reptiles in Israel. Israel Journal of Zoology 34, 77–90.Google Scholar
Ducloux, M. L. (1904). Sur une hémogrégarine de Emys leprosa . Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie. Paris 56, 564–565.Google Scholar
Fritz, U. and Havaš, P. (2007). Checklist of chelonians of the world. Vertebrate Zoology 57, 149–368.CrossRefGoogle Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.Google Scholar
Hahn, C. W. (1909). The stages of Haemogregarina stepanovi Danilewsky found in the blood of turtles, with special reference to ganges in the nucleus. Archiv für Protistenkunde 17, 307–376.Google Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Iverson, J. B. (1992). A Revised Checklist with Distribution Maps of the Turtles of the World. Privately printed, Richmond, IN, USA.Google Scholar
Kopečná, J., Jirků, M., Oborník, M., Tokarev, Y. S., Lukeš, J. and Modrý, D. (2006). Phylogenetic analysis of coccidian parasites from invertebrates: search for missing links. Protist 157, 173–183.Google Scholar
Kubo, M., Uni, S., Agatsuma, T., Nagataki, M., Panciera, R. J., Tsubota, T., Nakamura, S., Sakai, H., Masegi, T. and Yanai, T. (2008). Hepatozoon ursi n. sp. (Apicomplexa: Hepatozoidae) in Japanese black bear (Ursus thibetanus japonicus). Parasitology International 57, 287–294.CrossRefGoogle Scholar
Kvičerová, J., Pakandl, M. and Hypša, V. (2008). Phylogenetic relationships among Eimeria spp. (Apicomplexa, Eimeriidae) infecting rabbits: evolutionary significance of biological and morphological features. Parasitology 135, 443–452.Google Scholar
Landau, I. (1974). Hypothèses sur la phylogénie des Coccidiomorphes de Vertébrés. Zeitschrift für Parasitenkunde 45, 63–75.Google Scholar
Laveran, A. and 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.Google Scholar
Levine, N. D. (1988). The Protozoan Phylum Apicomplexa. CRC Press, Boca Raton, FL, USA.Google Scholar
Mathew, J. S., Van Den Bussche, R. A., Ewing, S. A., Malayer, J. R., Latha, B. R. and Panciera, R. J. (2000). Phylogenetic relationships of Hepatozoon (Apicomplexa: Adeleorina) based on molecular, morphologic, and life-cycle characters. Journal of Parasitology 86, 366–372.Google Scholar
Mihalca, A., Achelaritei, D. and Popescu, P. (2002). Haemoparasites of the genus Haemogregarina in a population of European pond turtles (Emys orbicularis) from Dragasani, Valcea county, Romania. Scientia Parasitologica 2, 22–27.Google Scholar
Mihalca, A., Racka, K., Gherman, C. and Ionescu, D. T. (2008). Prevalence and intensity of blood apicomplexan infections in reptiles from Romania. Parasitology Research 102, 1081–1083.Google Scholar
Page, R. D. M. (1996). TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.Google Scholar
Paperna, I. (1989). Developmental cycle of chelonian haemogregarines in leeches with extra-intestinal multiple sporozoite oocysts and a note on the blood stages in the chelonian hosts. Diseases of Aquatic Organisms 7, 149–153.Google Scholar
Paterson, W. B. and Desser, S. S. (1976). Observations on Haemogregarina balli sp. n. from the common snapping turtle, Chelydra serpentina . Journal of Protozoology 23, 294–301.Google Scholar
Perkins, F. O., Barta, J. R., Clopton, R. E., Pierce, M. A. and Upton, S. J. (2000). Phylum Apicomplexa; family Eimeriidae. In The Illustrated Guide to the Protozoa, 2nd Edn. (ed. Lee, J. J., Leedale, G. F. and Bradbury, P.), pp. 318–339. Allen Press Inc., Lawrence, KS, USA.Google Scholar
Rambaut, A. and Drummond, A. J. (2007). Tracer v1.4. httpTracerv1.4. http://beast.bio.ed.ac.uk/Tracer.Google Scholar
Reichenow, E. (1910). Haemogregarina stepanowi. Die Entwicklungsgeschichte einer Hämogregarine. Archiv für Protistenkunde 20, 251–350.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Roudabush, R. and Coatney, G. R. (1937). On some blood protozoa of reptiles and amphibians. Transactions of the American Microscopical Society 56, 291–297.Google Scholar
Siddall, M. E. (1995). Phylogeny of adeleid blood parasites with a partial systematic revision of the haemogregarine complex. Journal of Eukaryotic Microbiology 42, 116–125.Google Scholar
Siddall, M. E. and 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.Google Scholar
Siddall, M. E. and Desser, S. S. (1992). Prevalence and intensity of Haemogregarina balli (Apicomplexa: Adeleina: Haemogregarinidae) in tree turtle species from Ontario, with observations on intraerythrocytic development. Canadian Journal of Zoology 70, 123–128.CrossRefGoogle Scholar
Sloboda, M., Kamler, M., Bulantová, J., Votýpka, J. and Modrý, D. (2007). A new species of Hepatozoon (Apicomplexa: Adeleorina) from Python regius (Serpentes: Pythonidae) and its experimental transmission by a mosquito vector. Journal of Parasitology 93, 1189–1198.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.Google Scholar
Telford, S. R. (2009). Hemoparasites of the Reptilia: Color Atlas and Text. CRC Press, Boca Raton, FL, USA.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties, and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle Scholar
Wozniak, E. J., Telford, S. R. and McLaughlin, G. L. (1994). Employment of the Polymerase Chain Reaction in the molecular differentiation of reptilian hemogregarines and its application to preventive zoological medicine. Journal of Zoo and Wildlife Medicine 25, 538–547.Google Scholar
Xiao, L., Escalante, L., Yang, C., Sulaiman, I., Escalante, A. A., Montali, R. J., Fayer, R. and Lal, A. A. (1999). Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Applied and Environmental Microbiology 65, 1578–1583.Google Scholar