Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-18T14:00:46.833Z Has data issue: false hasContentIssue false

Reassignment of the land tortoise haemogregarine Haemogregarina fitzsimonsi Dias 1953 (Adeleorina: Haemogregarinidae) to the genus Hepatozoon Miller 1908 (Adeleorina: Hepatozoidae) based on parasite morphology, life cycle and phylogenetic analysis of 18S rDNA sequence fragments

Published online by Cambridge University Press:  13 June 2014

COURTNEY A. COOK*
Affiliation:
Department of Zoology, University of Johannesburg, P.O. Box 524, Auckland Park, 2006, Johannesburg, South Africa Water Research Group (Ecology), Unit for Environmental Sciences and Management, North West University, Potchefstroom, 2520, South Africa
SCOTT P. LAWTON
Affiliation:
School of Life Sciences, Kingston University, London KT1 2EE, UK
ANGELA J. DAVIES
Affiliation:
Water Research Group (Ecology), Unit for Environmental Sciences and Management, North West University, Potchefstroom, 2520, South Africa School of Life Sciences, Kingston University, London KT1 2EE, UK
NICO J. SMIT
Affiliation:
Water Research Group (Ecology), Unit for Environmental Sciences and Management, North West University, Potchefstroom, 2520, South Africa
*
*Corresponding author: Water Research Group (Ecology), Unit for Environmental Sciences and Management, North West University, Private Bag X6001, Potchefstroom, 2520, South Africa. E-mail: [email protected]

Summary

Research was undertaken to clarify the true taxonomic position of the terrestrial tortoise apicomplexan, Haemogregarina fitzsimonsi (Dias, 1953). Thin blood films were screened from 275 wild and captive South African tortoises of 6 genera and 10 species between 2009–2011. Apicomplexan parasites within films were identified, with a focus on H. fitzsimonsi. Ticks from wild tortoises, especially Amblyomma sylvaticum and Amblyomma marmoreum were also screened, and sporogonic stages were identified on dissection of adult ticks of both species taken from H. fitzsimonsi infected and apparently non-infected tortoises. Parasite DNA was extracted from fixed, Giemsa-stained tortoise blood films and from both fresh and fixed ticks, and PCR was undertaken with two primer sets, HEMO1/HEMO2, and HepF300/HepR900, to amplify parasite 18S rDNA. Results indicated that apicomplexan DNA extracted from tortoise blood films and both species of tick had been amplified by one or both primer sets. Haemogregarina  fitzsimonsi 18S rDNA sequences from tortoise blood aligned with those of species of Hepatozoon, rather than those of species of Haemogregarina or Hemolivia. It is recommended therefore that this haemogregarine be re-assigned to the genus Hepatozoon, making Hepatozoon fitzsimonsi (Dias, 1953) the only Hepatozoon known currently from any terrestrial chelonian. Ticks are its likely vectors.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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. (1991). The Dactylosomatidae. Advances in Parasitology 30, 137.Google Scholar
Barta, J. R., Ogendengbe, 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.Google Scholar
Boycott, R. C. and Bourquin, O. (2000). The Southern African Tortoise Book: A Guide to Southern African Tortoises, Terrapins and Turtles. O. Bourquin, Hilton, South Africa.Google Scholar
Branch, B. (1998). Field Guide to Snakes and Other Reptiles of Southern Africa. Struik Publishers, Cape Town, South Africa.Google Scholar
Branch, B. (2008). Tortoises, Terrapins and Turtles of Africa. Struik Publishers, Cape Town, South Africa.Google Scholar
Brumpt, E. (1938). Formes évolutives d'Haemogregarina mauritanica chez la tique Hyalomma syriacum. Annals of Parasitology 16, 350361.Google Scholar
Cook, C. A., Smit, N. J. and Davies, A. J. (2009). A redescription of Haemogregarina fitzsimonsi Dias, 1953 and some comments on Haemogregarina parvula Dias, 1953 (Adeleorina: Haemogregarinidae) from southern African tortoises (Cryptodira: Testudinidae), with new host data and distribution records. Folia Parasitologica 56, 173179.Google Scholar
Cook, C. A., Smit, N. J. and Davies, A. J. (2010). Hemoproteids (Apicomplexa: Haemoproteidae) from South African tortoises (Cryptodira: Testudinidae). Journal of Parasitology 96, 11681172.Google Scholar
Cook, C. A., Smit, N. J. and Davies, A. J. (in press). First record of an intraleucocytic haemogregarine (Adeleorina: Haemogregarinidae) from South African tortoises of the species Stigmochelys pardalis (Cryptodira: Testudinidae). African Zoology.Google Scholar
Davies, A. J. and Johnston, M. R. L. (2000). The biology of some intra-erythrocytic parasites of fishes, amphibians and reptiles. Advances in Parasitology 45, 1107.Google Scholar
Dias, J. A. T. S. (1953). Subsídios para o estudo dos hematozoários dos répteis de Moçambique. Boletim da Sociedade de Estudos Moçambique 23, 4173.Google Scholar
Edwards, K. T., Goddard, J. and Varela-Stokes, A. S. (2009). Examination of the internal morphology of the Ixodid tick, Amblyomma maculatum Koch, (Acari: Ixodidae); “How to” pictorial dissection guide. Midsouth Entomology 2, 2839.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
Harris, D. J., Gracia, E., Jorge, F., Maia, J. P. M. C., Perera, A., Carretero, M. A. and Gimenez, A. (2013). Molecular detection of Hemolivia (Apicomplexa: Haemogregarinidae) from ticks of North African Testudo graeca (Testudines: Testudinidae), and an estimation of their phylogenetic relationships using 18S rRNA sequences. Journal of Comparative Parasitology 80, 292296.Google Scholar
Herbert, J. D. K., Godfrey, S. S., Bull, C. M. and Menz, R. I. (2010). Developmental stages and molecular phylogeny of Hepatozoon tuatarae, a parasite infecting the New Zealand tuatara, Sphenodon punctatus and the tick, Amblyomma sphenodonti. International Journal of Parasitology 40, 13111315.CrossRefGoogle ScholarPubMed
Howell, C. J., Walker, J. B. and Nevill, E. M. (1978). Ticks, Mites and Insects Infesting Domestic Animals in South Africa, Part 1, Descriptions and Biology. Republic of South Africa, Department of Agricultural Technical Services, Science Bulletin 393, Government Printer, Pretoria, South Africa.Google Scholar
Landau, I. and Paperna, I. (1997). The assignment of Hepatozoon mauritanicum, a tick-transmitted parasite of tortoises, to the genus Hemolivia. Parasite 4, 365367.Google Scholar
McArthur, S., Wilkinson, R. and Meyer, J. (2004). Medicine and Surgery of Tortoises and Turtles. Blackwell Publishing, Oxford, UK.Google Scholar
Michel, J. C. (1973). Hepatozoon mauritanicum (Et. Et Ed. Sergent, 1904) n. comb., parasite de Testudo graeca: redescription de la sporogonie chez Hyalomma aeygyptium et de la schizogonie tissulaire d'après de materiel d'E. Brumpt. Annals of Parasitology 48, 1121.Google Scholar
Paperna, I. (2006). Hemolivia mauritanica (Haemogregarinidae: Apicomplexa) infection in the tortoise Testudo graeca in the near East with data on sporogonous development in the tick vector Hyalomma aegyptium. Parasite 13, 267273.Google Scholar
Perkins, S. L. and Keller, A. K. (2001). Phylogeny of nuclear small subunit rRNA genes of haemogregarines amplified with specific primers. Journal of Parasitology 87, 870876.Google Scholar
Petit, G., Landau, I., Baccam, D. and Lainson, R. (1990). Description et cycle biologique d'Hemolivia stellata n. g., n. sp., hémogrégarine de crapauds brésiliens. Annales de Parasitologie Humaine et Comparee 65, 315.Google Scholar
Sergent, E. and Sergent, E. (1904). Sur une hémogrégarine, parasite de Testudo mauritanica. Comptes Rendus des Seances de la Societe de Biologie et de ses Filiales 56, 130131.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
Široký, P., Kamler, M. and Modrý, D. (2004). Long-term occurrence of Hemolivia cf. mauritanica (Apicomplexa: Adeleina: Haemogregarinidae) in captive Testudo marginata (Reptilia: Testudinidae): evidence for cyclic merogony? Journal of Parasitology 90, 13911393.Google Scholar
Široký, P., Kamler, M., Frye, F. L., Fictum, P. and Modrý, D. (2007). Endogenous development of Hemolivia mauritanica (Apicomplexa: Adeleina: Haemogregarinidae) in the marginated tortoise Testudo marginata (Reptilia: Testudinidae): evidence from experimental infection. Folia Parasitologica 54, 1318.Google Scholar
Smith, T. G. (1996). The genus Hepatozoon (Apicomplexa: Adeleina). Journal of Parasitology 82, 565585.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, New York, NY, USA.Google Scholar
Telford, S. R., Wozniak, E. J. and Butler, J. F. (2001). Haemogregarine specificity in two communities of Florida snakes, with descriptions of six new species of Hepatozoon (Apicomplexa: Hepatozoidae) and a possible species of Haemogregarina (Apicomplexa: Haemogregarinidae). Journal of Parasitology 87, 890905.CrossRefGoogle Scholar
Tetley, L., Brown, S. M. A., McDonald, V. and Coombs, G. H. (1998). Ultrastructural analysis of the sporozoite of Cryptosporidium parvum. Microbiology 144, 32493255.Google Scholar
Ujvari, B., Madsen, T. and Olsson, M. (2004). High prevalence of Hepatozoon spp. (Apicomplexa: Hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia. Journal of Parasitology 90, 670672.Google Scholar
Van As, J., Davies, A. J. and Smit, N. J. (2013). Hepatozoon langii n. sp. and Hepatozoon vacuolatus n. sp. (Apicomplexa: Adeleorina: Hepatozoidae) from the crag lizard (Sauria: Cordylidae) Pseudocordylus langi from the North Eastern Drakensberg escarpment, Eastern Free State, South Africa. Zootaxa 3608, 345356.Google Scholar
Vilcins, I. E., Ujvari, B., Old, J. M. and Deane, E. (2009). Molecular and morphological description of a Hepatozoon species in reptiles and their ticks in the Northern Territory, Australia. Journal of Parasitology 5, 434442.Google Scholar