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Haemogregarines of freshwater turtles from Southeast Asia with a description of Haemogregarina sacaliae sp. n. and a redescription of Haemogregarina pellegrini Laveran and Pettit, 1910

Published online by Cambridge University Press:  04 March 2015

NELA DVOŘÁKOVÁ
Affiliation:
Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, 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:
Biology Centre, Academy of Sciences of the Czech Republic, Institute of Parasitology, Branišovská 31, 370 05 České Budějovice, Czech Republic Department of Parasitology, Faculty of Science, University of South Bohemia, Branišovská 1760, 370 05 České Budějovice, Czech Republic
MARTIN HOSTOVSKÝ
Affiliation:
Department of Biochemistry, Biophysics and Chemistry, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1/3, 612 42 Brno, Czech Republic
PAVEL ŠIROKÝ*
Affiliation:
Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, 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 Brno, Palackého tř. 1/3, 612 42 Brno, Czech Republic. E-mail: [email protected]

Summary

The uniform morphology of the developmental stages of Haemogregarina species and the insufficient information supplied by the simplistic descriptions of previous authors complicates their differential diagnosis and proper species identification. In this study, we detected Haemogregarina spp. in 6 out of 22 (27·2%) examined turtles originating from Southeast Asia, Malayemys subtrijuga (n = 4), Sacalia quadriocellata (n = 1) and Platysternon megacephalum (n = 1), and compared them with the available literature data. Microscopic analysis of our isolates distinguished 2 morphological species, Haemogregarina pellegrini and one new species, being described in this paper as Haemogregarina sacaliae sp. n. Phylogenetic analyses based on 1210 bp long fragment of 18S rDNA sequences placed both haemogregarines firmly within the monophyletic Haemogregarina clade. Isolates of H. pellegrini from 2 distantly related turtle hosts, M. subtrijuga and P. megacephalum, were genetically identical. Despite the fact that numerous Haemogregarina species of turtles have been described, the incompleteness of the morphological data and relatively low host specificity provides the space for large synonymy within this taxon. Therefore, a complex approach combining microscopic analyses together with molecular-genetic methods should represent the basic standard for all taxonomic studies.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Acholonu, A. D. (1974). Haemogregarine pseudemydis n. sp. (Apicomplexa: Haemogregarinidae) and Pirhemocyton chelonarium n. sp. in turtles from Lousiana. Journal of Protozoology 21, 659664.Google Scholar
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, 171180.CrossRefGoogle ScholarPubMed
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, 731738.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, 899904.Google Scholar
Castellani, A. and Willey, A. (1905). Observations on haematozoa in Ceylon. Quarterly Journal of Microscopical Science 49, 383402.Google Scholar
Chai, J. Y. and Chen, C. H. (1990). Six new species of Haemogregarina from Chinese turtles. Acta Hydrobiologica Sinica 14, 129137.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, 9399.Google Scholar
Davis, A. K. and Sterrett, S. C. (2011). Prevalence of Haemogregarine parasites in three freshwater turtle species in a population in Northeast Georgia, USA. International Journal of Zoological Research 7, 156163.Google Scholar
Desser, S. S. (1993). The Haemogregarinidae and Lankesterellidae. In Parasitic Protozoa, (ed. Kreier, J. P.), pp. 247272. Vol. 4. 2nd Edn., Academic Press, New York, USA.Google Scholar
Dvořáková, N., Kvičerová, J., Papoušek, I., Javanbakht, H., Tiar, G., Kami, H. and Široký, P. (2014). Haemogregarines from western Palaearctic freshwater turtles (genera Emys, Mauremys) are conspecific with Haemogregarina stepanowi Danilewsky, 1885. Parasitology 141, 522530.Google Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.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, 9598.Google Scholar
Hossen, M. S., Bandyopadhyay, P. K. and Gürelli, G. (2013). On the occurrence of a Haemogregarinae (Apicomplexa) parasite from freshwater turtles of South 24 Parganas, West Bengal, India. Türkiye Parazitoloji Dergisi 37, 118122.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, 173183.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, 287294.Google 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, 443452.Google Scholar
Kvičerová, J., Hypša, V., Dvořáková, N., Mikulíček, P., Jandzik, D., Gardner, M. G., Javanbakht, H., Tiar, G. and Široký, P. (2014). Hemolivia and Hepatozoon: haemogregarines with tangled evolutionary relationships. Protist 165, 688700.Google Scholar
Laveran, A. and Mesnil, F. (1902). Sur quelques protozoaires parasites d'une tortue d'Asie (Damonia reevesii). Comptes Rendus de l'Academie des Sciences, Series 3, 609614.Google Scholar
Laveran, A. and Nattan-Larrier, L. A. A. (1912). Sur une hémogrégarine de Testudo emys . Comptes Rendus des séances de la Société de Biologie 72, 134136.Google Scholar
Laveran, A. and Pettit, A. (1910). Sur une hemogregarine nouvelle de Damonia subtrijuga Schlegel. Comptes rendus de l'Académie des Sciences 151, 10171019.Google Scholar
Levine, N. D. (1988). The Protozoan Phylum Apicomplexa. CRC Press, Boca Raton, Florida.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, 366372.Google Scholar
McAuliffe, J. R. (1977). A hypothesis explaining variations of hemogregarine parasitemia in different aquatic turtle species. Journal of Parasitology 63, 580581.Google Scholar
McCoy, J. C., Failey, E. L., Price, S. J. and Dorcas, M. E. (2007). An assessment of leech parasitism on semi-aquatic turtles in the western piedmont of North Carolina. Southeastern Naturalist 6, 191202.Google Scholar
Mello de, F. (1932a). Contribution à l'étude des hémogrégarinides des tortues indiennes. I. Haemogregarina malabarica n. sp. et son cycle évolutif chez Emyda granosa, subspecies vittata Peters. Arquivos da Escola Médico-Cirurgica de Nova Goa – Série A 8, 14111425, Plates I–II.Google Scholar
Mello de, F. (1932b). Contribution à l'étude des hémogrégarinides des tortues indiennes. II. Sur une Hémogrégarine parasite de Emyda granosa Schoepf. Arquivos da Escola Médico-Cirurgica de Nova Goa – Série A 8, 14261431. Plates II–IV.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, 2227.Google Scholar
Misra, K. K. (1976). Haemogregarina gangetica a new name for Haemogregarina simondi of a river turtle, Trionyx gangeticus . Acta Protozoologica 15, 2122.Google Scholar
Misra, K. K., Nandi, N. C., Raut, S. and Choudhury, A. (1974). Haemogregarina simondi n. sp. a new haemogregarine from a river turtle, Trionyx gangeticus Cuvier. Acta Protozoologica 12, 2122.Google Scholar
Page, R. D. M. (1996). TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357358.Google Scholar
Paterson, W. B. and Desser, S. S. (1976). Observations of Haemogregarina balli sp. n. from the common snapping turtle, Chelydra serpentina . Journal of Protozoology 23, 294301.CrossRefGoogle Scholar
Patton, W. S. (1908). The haemogregarines of mammals and reptiles. Parasitology 1, 318321.CrossRefGoogle Scholar
Perkins, S. L. and Keller, A. K. (2001). Phylogeny of nuclear small subunit rRNA genes of hemogregarines amplified with specific primers. Journal of Parasitology 87, 870876.Google Scholar
Prowazek, S. (1910). Parasitische Protozoen aus Japan, gesammelt von Herrn Dr. Mine in Fukuoka. Archiv für Schiffs- und Tropen-Hygiene 14, 296302.Google Scholar
Ray, R. and Bhattacharjee, A. (1984). Haemogregarina choudhuryi sp. n. (Apicomplexa: Haemogregarinidae) in common pond water turtle, Lissemys punctata punctata (Bonnaterre) from West Bengal. Acta Protozoologica 23, 6774.Google Scholar
Reichenow, E. (1910). Haemogregarina stepanowi. Die Entwicklungsgeschichte einer Hamogregarine. Archiv für Protistenkunde 20, 251350.Google Scholar
Robertson, M. (1908). A preliminary note on haematozoa from Ceylon reptiles. Spolia Zeylanica 5, 178185.Google Scholar
Robertson, M. (1910). Studies on Ceylon haematozoa. No. II – Notes on the life cycle of Haemogregarina nicoriae, Cast and Willey. The Quarterly Journal of Microscopical Science 55, 741762.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.Google Scholar
Saratchandra, B. (1981). Two new haemogregarines, Haemogregarina waltairensis n. sp. from Calotes versicolor (Daudin) and H. ganapatii n. sp. from Lissemys punctata (Shoepff). Animal Science 90, 365371.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, 116125.Google Scholar
Siddall, M. E. and 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, 123128.CrossRefGoogle Scholar
Simond, P. L. (1901). Contribution al'etude des hematozoires endoglobulaires des reptiles. Annales de l'Institut Pasteur 15, 319351.Google Scholar
Sinha, C. K. (1993). A new Haemogregarina from a freshwater turtle of West Bengal. Geobios New Reports 121, 510.Google Scholar
Široký, P., Kamler, M. and Modrý, D. (2005). Prevalence of Hemolivia mauritanica (Apicomplexa: Adeleina: Haemogregarinidae) in natural populations of tortoises of the genus Testudo in the east Mediterranean region. Folia Parasitologica 52, 359361.Google 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, 11891198.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2001). Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sinauer Associates, Sunderland, MA.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, 27312739.Google Scholar
Telford, S. R. (2009). Hemoparasites of the Reptilia: Color Atlas and Text. CRC Press, Boca Raton.Google Scholar
Telford, S. R., Norton, T. M., Moler, P. E. and Jensen, J. B. (2009). A new Haemogregarina species of the alligator snapping turtle, Macrochelys temminckii (Testudines: Chelydridae), in Georgia and Florida that produces macromeronts in circulating erythrocytes. Journal of Parasitology 95, 208214.CrossRefGoogle ScholarPubMed
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, 46734680.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, 15781583.Google Scholar