Harmless parasites? Infections with Hemolivia mauritanica (Apicomplexa: Adeleorina: Karyolysidae) and Haemocystidium spp. (Apicomplexa: Haemosporida: Haemoproteidae) have a negligible impact on white cell counts in tortoise hosts
Jazyk angličtina Země Česko Médium electronic
Typ dokumentu časopisecké články
PubMed
41392952
DOI
10.14411/fp.2025.031
PII: 2025.031
Knihovny.cz E-zdroje
- Klíčová slova
- blood parasites, differential leucocyte count, haemogregarine, haemosporidia, mitotic erythrocyte, polychromatophil, reptiles,
- MeSH
- Apicomplexa * fyziologie MeSH
- Haemosporida * fyziologie MeSH
- leukocyty MeSH
- parazitemie veterinární parazitologie MeSH
- počet leukocytů veterinární MeSH
- protozoální infekce zvířat * parazitologie krev MeSH
- želvy * parazitologie MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
The pathogenicity of haemogregarines and their effects on the health status of ectothermic hosts remain largely unexplored. In this study, we examined the impact of Hemolivia mauritanica (Sergent et Sergent, 1904) infection on the differential leukocyte count (DLC) as a measurable indicator of health in tortoise hosts. A total of 206 blood smears were analysed, including 181 from spur-thighed tortoises (Testudo graeca Linnaeus) and 25 from marginated tortoises (Testudo marginata Schoepff). Light microscopy was used to identify infected individuals, determine DLC, and quantify parasitaemia levels. Overall, H. mauritanica was detected in 125 of 181 (69%) T. graeca samples and 21 of 25 (84%) T. marginata samples. To assess whether infection influenced DLC, we statistically compared leukocyte profiles between infected and uninfected individuals. Additionally, we evaluated the effects of other factors, including host species, parasitaemia intensity, sex, age, and the month and year of blood collection. Wilcoxon rank-sum tests revealed that parasitaemia and age had a statistically significant effect on DLC in T. graeca. Further analysis using linear models showed a significant association between parasitaemia and DLC, specifically affecting azurophils in T. graeca and basophils in T. marginata. Nine T. graeca tortoises positive for H. mauritanica were co-infected with haemosporidian parasites of the genus Haemocystidium Castellani et Willey, 1904, specifically three with Haemocystidium anatolicum (Orkun et Güven, 2013) and six with Haemocystidium caucasicum (Krasilnikov, 1965). Although co-infection itself was not statistically significant, a separate analysis of Haemocystidium parasitaemia revealed a significant effect on lymphocyte DLC. Furthermore, the frequent presence of mitotic and polychromatophilous erythrocytes in H. mauritanica-infected tortoises suggests a potential increase in erythrocyte regeneration.
Department of Biology Faculty of Science University of Guilan Rasht Iran
Department of Zoology Faculty of Natural Sciences Comenius University in Bratislava Slovakia
Veterinary Office for Birds of Prey and Exotic Birds Prague Czech Republic
Zobrazit více v PubMed
Ali A.F., Ali A.O., Fawaz M.M., Mohamed A.E. 2018: Hematological and parasitological investigation in Testudo graeca (Linnaeus, 1758) tortoise kept in captivity in Egypt. Kafrelsheikh Vet. Med. J. 16: 45-60. DOI
Apache J., Rodríguez-Almonacid C.C., Moreno-Torres C.A., Gamboa-Suárez B.A., Matta N.E. 2023: Hemoparasite occurrence and hematological/serum chemistry variations in Podocnemis vogli turtles: a comparative analysis between wild-residing infected specimens and captive non-infected counterparts. Vet. Parasitol. Reg. Stud. Reports 45: 100928. PubMed DOI
Arikan H., Çiçek K. 2014: Haematology of amphibians and reptiles: a review. North-West. J. Zool. 10: 190-290.
Barradas P.F., Lima C., Cardoso C., Amorim I., Gärtner F., Mesquita J.R. 2021: Molecular evidence of Hemolivia mauritanica, Ehrlichia spp. and the endosymbiont Candidatus Midichloria mitochondrii in Hyalomma aegyptium infesting Testudo graeca tortoises from Doha, Qatar. Animals (Basel) 11: 30. PubMed DOI
Barton K. 2020. MuMIn: Multi-Model Inference. R package version 1.43.17. Available from: https://CRAN.R-project.org/package=MuMIn
Bielli M., Nardini G., Di Girolamo N., Savarino P. 2015: Hematological values for adult eastern Hermann´s tortoise (Testudo hermanni boettgeri) in semi-natural conditions. J. Vet. Diagn. Invest. 27: 67-73 PubMed DOI
Bower D.S., Brannelly L.A., McDonald C.A., Webb R.J., Greenspan S.E., Vickers M., Gardner M.G., Greenlees M.J. 2019: A review of the role of parasites in the ecology of reptiles and amphibians. Austr. Ecol. 44: 433-448. DOI
Brumpt E. 1938: Formes évolutives d'Haemogregarina mauritanica chez la tique Hyalomma syriacum. Ann. Parasitol. 16: 350-361. DOI
Casal A.B., Camacho M., López-Jurado L.F., Juste C., Orós J. 2009: Comparative study of hematologic and plasma biochemical variables in eastern Atlantic juvenile and adult nesting loggerhead sea turtles (Caretta caretta). Vet. Clin. Pathol. 38: 213-218. PubMed DOI
Cavalcante M.C., Chagas-de-Souza D., Coêlho T.A., Viana L.A., Adriano E., Corrêa L.L. 2024: Hemoparasite analysis and hematological parameters of four freshwater turtle species(Testudines: Podocnemididae) from the Brazilian Amazon. Acta Parasitol. 69: 1058-1066. PubMed DOI
Eatwell K., Hedley J., Barron R. 2014: Reptile haematology and biochemistry. In Pract. 36: 34-42. DOI
Fritz U. 2001: Handbuch der Reptilien und Amphibien Europas. Band 3/IIIA Schildkröten (Testudines) I (Bataguridae, Testudinidae, Emydidae). AULA-Verlag GmbH, Wiebelsheim, Germany, 594 pp.
Fritz U., Harris D.J., Fahd S., Rouag R., Graciá Martínez E., Giménez Casalduero A., Široký P., Kalboussi M., Jdeidi T.B., Hundsdörfer A.K. 2009: Mitochondrial phylogeography of Testudo graeca in the Western Mediterranean: old complex divergence in North Africa and recent arrival in Europe. Amphib. - Reptil. 30: 63-80. DOI
Fritz U., Hundsdörfer A.K., Široký P., Auer M., Kami H., Lehman J., Mazaneva L.F., Türkozan O., Wink M. 2007: Phenotypic plasticity leads to incongruence between morphology-based taxonomy and genetic differentiation in western Palaearctic tortoises (Testudo graeca complex; Testudines, Testudinidae). Amphib. - Reptil. 28: 97-121. DOI
Galen S.C., Borner J., Martinsen E.S., Schaer J., Austin C.C., West J., Perkins S.L. 2018: The polyphyly of Plasmodium: comprehensive phylogenetic analyses of the malaria parasites (order Haemosporida) reveal widespread taxonomic conflict. R. Soc. Open Sci. 5: 171780. PubMed DOI
González L.P., Vargas-León C.M., Fuentes-Rodríguez G.A., Calderón-Espinosa M.L., Matta N.E. 2021: Do blood parasites increase immature erythrocytes and mitosis in amphibians? Rev. Biol. Trop. 69: 615-625. DOI
Halla U., Korbel R., Mutschmann F., Rinder M. 2014: Blood parasites in reptiles imported to Germany. Parasitol. Res. 113: 4587-4599. PubMed DOI
Hananeh W.M., Radhi A., Mukbel R.M., Ismail Z.B. 2022: Effects of parasites coinfection with other pathogens on animal host: a literature review. Vet. World. 15: 2414-2424. PubMed DOI
Hernández J.D., Castro P., Saavedra P., Ramírez P., Orós J. 2017: Morphologic and cytochemical characteristics of the blood cells of the yellow-bellied slider (Trachemys scripta scripta). Anat. Histol. Embryol. 46: 446-455. PubMed DOI
Jacobson E.R., Garner M.M. 2021: Infectious Diseases and Pathology of Reptiles. CRC Press, Boca Raton, 1030 pp. DOI
Javanbakht H., Ihlow F., Jablonski D., Široký P., Fritz U., Rödder D., Sharifi M., Mikulíček P. 2017: Genetic diversity and Quaternary range dynamics in Iranian and Transcaucasian tortoises. Biol. J. Linn. Soc. 121: 627-640. DOI
Javanbakht H., Kvičerová J., Dvořáková N., Mikulíček P., Sharifi M., Kautman M., Maršíková A., Široký P. 2015a: Phylogeny, diversity, distribution, and host specificity of Haemoproteus spp. (Apicomplexa: Haemosporida: Haemoproteidae) of Palaerctic tortoises. J. Eukaryot. Microbiol. 62: 670-678. PubMed DOI
Javanbakht H., Široký P., Mikulíček P., Sharifi M. 2015b: Distribution and abundance of Hemolivia mauritanica (Apicomplexa: Haemogregarinidae) and its vector Hyalomma aegyptium in tortoises of Iran. Biologia. 70: 229-234. DOI
Knotkova Z., Mazanek S., Hovorka M., Sloboda M., Knotek Z. 2005: Haematology and plasma chemistry of Bornean river turtles suffering from shell necrosis and haemogregarine parasites. Vet. Med. 50: 421-426. DOI
Krasilnikov E.N. 1965: Blood parasites of turtles of southeast Georgia. Zool. Zh. 44: 1454-1459. (In Russian.)
Kvičerová J., Hypša V., Dvořáková N., Mikulíček P., Jandzik D., Gardner M.G., Javanbakht H., Tiar G., Široký P. 2014: Hemolivia and Hepatozoon: haemogregarines with tangled evolutionary relationships. Protist 165: 688-700. PubMed DOI
Laghzaoui E.-M., Sergiadou D., Perera A., Harris D.J., Abbad A., El Mouden E.H. 2020: Absence of Hemolivia mauritanica (Apicomplexa: Haemogregarinidae) in natural populations of Testudo graeca in Morocco. Parasitol. Res. 119: 4281-4286. PubMed DOI
Landau I., Paperna I. 1997: The assignment of Hepatozoon mauritanicum, a tick-transmitted parasite of tortoise, to the genus Hemolivia. Parasite 4: 365-367. DOI
Martínez-Silvestre A., Arribas O. 2014: Blood differential count and effect of haemoparasites in wild populations of Pyrenean lizard Iberolacerta aurelioi (Arribas, 1994). Basic Appl. Herpetol. 28: 79-86. DOI
Martínez-Silvestre A., Lavín S., Cueca R. 2011: Hematología y citología sanguínea en reptiles. Clin. Vet. Pequeños Animales 31: 131-141.
Martínez-Silvestre A., Lavin S., Marco I., Montane J., Ramon Lopez J., Soler Massana J. 2001: Haematology and plasma chemistry of captive Testudo marginata. Proceedings of the International Congress on Testudo Genus, Gonfaron, 7-10 March 2001. Chelonii 3: 187-189.
Martínez-Silvestre A., Mateu de Antonio E., Ramis A., Majó N. 1999: Etiología y descripción clínica de la rinitis crónica en tortuga mora (Testudo graeca). Rev. Esp. Herp. 13: 27-36.
Martins G.S., Alevi K.C.C., Azeredo-Oliveira M.T.V., Bonini-Domingos C.R. 2016: Cytochemical characteristics of blood cells from Brazilian tortoises (Testudines: Testudinidae). Genet. Mol. Res. 15: 15017549. PubMed DOI
Michel J. C. 1973: Hepatozoon mauritanicum (Et. et Ed. Sergent, 1904) n. comb., parasite de Testudo graeca: redescription de la sporogonie chez Hyalomma aegyptium et de la schizogonie tissulaire d'après le matériel d'E. Brumpt. Ann. Parasitol. Hum. Comp. 48: 11-21. PubMed DOI
Mihalca A., Achelaritei D., Popescu P. 2002: Haemoparasites of the genus Haemogregarina in a population of European pond turtles (Emys orbicularis) from Dragasani, Valcea County, Romania. Sci. Parasitol. 2: 22-27.
Mikulíček P., Jandzik D., Fritz U., Schneider C., Široký P. 2013: AFLP analysis shows high incongruence between genetic differentiation and morphology-based taxonomy in a widely distributed tortoise. Biol. J. Linn. Soc. 108: 151-160. DOI
Mollie E.B., Kristensen K., van Benthem K.J., Magnusson A., Berg C.W., Nielsen A., Skaug H.J., Maechler M., Bolker B.M. 2017: glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9: 378-400. DOI
Okon E.M., Okocha R.C., Taiwo A.B., Michael F.B., Bolanle A.M. 2023: Dynamics of co-infection in fish: a review of pathogen-host interaction and clinical outcome. Fish Shellfish Immunol. Rep. 4: 100096. PubMed DOI
Orkun O., Güven E. 2013: A new species of Haemoproteus from a tortoise (Testudo graeca) in Turkey, with remarks on molecular phylogenetic and morphological analysis. J. Parasitol. 99: 112-117. PubMed DOI
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: 267-273. PubMed DOI
Picelli A.M., de Carvalho A.V., Viana L.A., Malvasio A. 2015: Prevalence and parasitemia of Haemogregarina sp. in Podocnemis expansa (Testudines: Podocnemididae) from the Brazilian Amazon. Rev. Bras. Parasitol. Vet. 24: 191-197. PubMed DOI
Pineda-Catalan O., Perkins S.L., Peirce M.A., Engstrand R., Garcia-Davila C., Pinedo-Vasquez M., Aguirre A.A. 2013: Revision of hemoproteid genera and description and redescription of two species of chelonian hemoproteid parasites. J. Parasitol. 99: 1089-1098. PubMed DOI
Posit Team 2023: RStudio: Integrated Development Environment for R. Posit Software, PBC, Boston, MA. Available from: http://www.posit.co/.
Rataj A.V., Lindtner-Knific R., Vlahović K., Marvi U., Dovč A. 2011: Parasites in pet reptiles. Acta Vet. Scand. 53: 33-54. PubMed DOI
Rossow J.A., Hernandez S.M., Sumner S.M., Altman B.R., Crider C.G., Gammage M. B., Segal K.M., Yabsley M.J., 2013: Haemogregarine infections of three species of aquaticfreshwater turtles from two sites in Costa Rica. Int. J. Parasitol. Parasit. Wildlife 2: 131-135. PubMed DOI
Salakij C., Salakij J., Suthunmapinunta P., Chanhome L. 2002: Hematology, morphology and ultrastructure of blood cells and blood parasites from puff-faced watersnakes (Homalopsis buccata). Agric. Nat. Resour. 36: 35-43.
Schall J.J. 1990: Virulence of lizard malaria: the evolutionary ecology of an ancient parasite-host association. Parasitology. 100(S1): S35-S52. PubMed DOI
Sergent Ed., Sergent Et. 1904: Sur une hémogrégarine, parasite de Testudo mauritanica. Compt. Rend. Séances Mém. Soc. Biol. Fil. 56: 130-131.
Široký P., Jandzík D., Mikulíček P., Moravec J., Országh I. 2007b: Leptoconops bezzii (Diptera: Ceratopogonidae) parasitizing tortoises Testudo graeca (Testudines: Testudinidae) in mountain ranges of Lebanon and western Syria. Parasitol. Res. 101: 485-489. PubMed DOI
Široký P., Kamler M., Frye F.L., Fictum P., Modrý D. 2007a: Endogenous development of Hemolivia mauritanica (Apicomplexa: Adeleina: Haemogregarinidae) in the marginated tortoise Testudo marginata (Reptilia: Testudinidae): evidence from experimental infection. Folia Parasitol. 54: 13-18. DOI
Široký P., Kamler M., Modrý D. 2004: Long-term occurrence of Hemolivia cf. mauritanica (Apicomplexa: Adeleina: Haemogregarinidae) in captive Testudo marginata (Reptilia: Testudinidae): evidence for cyclic merogony? J. Parasitol. 90: 1391-1393. PubMed DOI
Široký P., Kamler M., 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 Parasitol. 52: 359-361. DOI
Široký P., Mikulíček P., Jandzík D., Kami H., Mihalca A.D., Rouag R., Kamler M., Schneider C., Záruba M., Modrý D. 2009: Co-distribution pattern of a haemogregarine Hemolivia mauritanica (Apicomplexa: Haemogregarinidae) and its vector Hyalomma aegyptium (Metastigmata: Ixodidae). J. Parasitol. 95: 728-733. PubMed DOI
Stacy N.I., Alleman A.R., Sayler K.A. 2011: Diagnostic hematology of reptiles. Clin. Lab. Med. 31: 87-108. PubMed DOI
Strik N.I., Alleman A.R., Harr K.E. 2007: Circulating inflammatory cells. In: E.R. Jacobson (Ed.), Infectious Diseases and Pathology of Reptiles. Colour Atlas and Text. CRC Press, Taylor & Francis, Boca Raton, pp. 167-218. DOI
Telford S.R. 1984: Haemoparasites of reptiles. In: G.L. Huff, F. Frye, E.R. Jacobson (Eds.), Diseases of Amphibians and Reptiles. Plenum Press, New York, pp. 385-517. DOI
Telford S.R. 2009: Hemoparasites of the Reptilia: Color Atlas and Text. CRC Press, Boca Raton, 376 pp.
Thumbi S.M., de C. Bronsvoort B.M., Poole E.J., Kiara H., Toye P., Ndila M., Conradie I., Jennings A., Handel I.G., Coetzer J.A., Hanotte O., Woolhouse M.E. 2013: Parasite co-infections show synergistic and antagonistic interactions on growth performance of East African zebu cattle under one year. Parasitology 140: 1789-1798. PubMed DOI
Venables W.N., Ripley B.D. 2002: Modern Applied Statistics with S. Fourth Edition. Springer, New York, 498 pp. DOI
Winter J.M., Stacy N.I., Adamovicz L.A., Allender M.C. 2019: Investigating the analytical variability and agreement of manual leukocyte quantification methods in Eastern box turtles (Terrapene carolina carolina). Front. Vet. Sci. 6: 398. PubMed DOI