Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-24T13:26:28.310Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogenetic relationship of Hepatozoon blood parasites found in snakes from Africa, America and Asia

Published online by Cambridge University Press:  30 October 2013

B. HAKLOVÁ ,
V. MAJLÁTHOVÁ ,
I. MAJLÁTH ,
D. J. HARRIS ,
V. PETRILLA ,
T. LITSCHKA-KOEN ,
M. OROS  and
B. PEŤKO
B. HAKLOVÁ*
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic
V. MAJLÁTHOVÁ
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic
I. MAJLÁTH
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic Institute of Biology and Ecology, University of P.J. Šafárik in Košice, Moyzesova 11, 040 01 Košice, Slovak Republic
D. J. HARRIS
Affiliation:
CI BIO-UP, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal
V. PETRILLA
Affiliation:
Department of Anatomy, Histology and Physiology, University of Veterinary Medicine and Pharmacy in Košice, Komenského 73, 041 81 Košice, Slovak Republic
T. LITSCHKA-KOEN
Affiliation:
Country club Simunye, P.O. Box 30, Simunye, Swaziland, Africa
M. OROS
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic
B. PEŤKO
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic
*
* Corresponding author: Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The blood parasites from the genus Hepatozoon Miller, 1908 (Apicomplexa: Adeleida: Hepatozoidae) represent the most common intracellular protozoan parasites found in snakes. In the present study, we examined 209 individuals of snakes, from different zoogeographical regions (Africa, America, Asia and Europe), for the occurrence of blood parasites using both molecular and microscopic examination methods, and assess phylogenetic relationships of all Hepatozoon parasites from snakes for the first time. In total, 178 blood smears obtained from 209 individuals, representing 40 species, were examined, from which Hepatozoon unicellular parasites were found in 26 samples (14·6% prevalence). Out of 180 samples tested by molecular method polymerase chain reaction (PCR), the presence of parasites was observed in 21 individuals (prevalence 11·6%): 14 snakes from Africa belonging to six genera (Dendroaspis, Dispholidus, Mehelya, Naja, Philothamnus and Python), five snakes from Asia from the genus Morelia and two snakes from America, from two genera (Coluber and Corallus). The intensity of infection varied from one to 1433 infected cells per 10 000 erythrocytes. Results of phylogenetic analyses (Bayesian and Maximum Likelihood) revealed the existence of five haplotypes divided into four main lineages. The present data also indicate neither geographical pattern of studied Hepatozoon sp., nor congruency in the host association.

Keywords

Hepatozoonsnakesvectorsphylogenetic analysesAfricaAmericaAsiaEurope
Type
Research Article
Information
Parasitology , Volume 141 , Issue 3 , March 2014 , pp. 389 - 398
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

Allen, D. E. and Little, T. J. (2009). Exploring the molecular landscape of host–parasite coevolution. Cold Spring Harbor Symposia on Quantitative Biology 74, 169–176.CrossRefGoogle ScholarPubMed
As, J. V., 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, 345–356. doi: 10.11646/zootaxa.3608.5.3.Google Scholar
Baker, J. R. (1974). Protozoan parasites of the blood of British wild birds and mammals. Journal of Zoology 172, 169–190. doi: 10.1111/j.1469-7998.1974.tb04100.x.CrossRefGoogle Scholar
Ball, G. H., Chao, J. and Telford, S. R. Jr. (1967). The life history of Hepatozoon rarefaciens (Sambon and Seligmann, 1907) from Drymarchon corais (Colubridae), and its experimental transfer to Constrictor constrictor (Boidae). Journal of Parasitology 53, 897–909. doi: 10.1016/S0003-9365(11)80154-5.CrossRefGoogle ScholarPubMed
Ball, G. H., Chao, J. and Telford, S. R. Jr. (1969). Hepatozoon fusifex sp. n., a hemogregarine from Boa constrictor producing marked morphological changes in infected erythrocytes. Journal of Parasitology 55, 800–813.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, 171–180. doi: 10.1111/j.1550-7408.2011.00607.x.CrossRefGoogle ScholarPubMed
Bashtar, A. R., Abdel-Ghaffar, F. A. and Shazly, M. A. (1987). Developmental stages of Hepatozoon gracilis (Wenyon, 1909) comb. nov., a parasite of the Egyptian skink, Mabuya quinquetaeniata . Parasitology Research 73, 507–514. doi: 10.1007/BF00535324.Google Scholar
Carini, A. (1909). Sur une Hemogregarine du Caiman latirostris Daud. Bulletin de la Société de Pathologie Exotique 2, 471–472.Google Scholar
Clark, G. M. (1958). Hepatozoon griseisciuri n. sp.; A new species of Hepatozoon from the grey squirrel (Sciurus carolinensis Gmelin, 1788), with studies on the life cycle. Journal of Parasitology 44, 52–63.Google Scholar
Criado-Fornelio, A., Ruas, J. L., Casado, N., Farias, N. A. R., Soares, M. P., Müller, G., Brum, J. G. W., Berne, M. E. A., Buling-Saraña, A. and Barba-Carretero, J. C. (2006). New molecular data on mammalian Hepatozoon species (Apicomplexa: Adeleorina) from Brazil and Spain. Journal of Parasitology 92, 93–99. doi: 10.1645/GE-464R.1.CrossRefGoogle ScholarPubMed
Criado-Fornelio, A., Rey-Valeiron, C., Buling, A., Barba-Carretero, J. C., Jefferies, R. and Irwin, P. (2007). New advances in molecular epizootiology of canine hematic protozoa from Venezuela, Thailand and Spain. Veterinary Parasitology 144, 261–269. doi: 10.1016/j.vetpar.2006.09.042.CrossRefGoogle ScholarPubMed
Criado-Fornelio, A., Buling, A., Casado, N., GIimenez, C., Ruas, J., Wendt, L., da Rosa-Farias, N., Pinheiro, M., Rey-Valeiron, C. and Barba-Carretero, J. C. (2009). Molecular characterization of arthropod-borne hematozoans in wild mammals from Brazil, Venezuela and Spain. Acta Parasitologica 54, 187–193. doi: 10.2478/s11686-009-0031-5.Google Scholar
Durrant, K. L., Beadell, J. S., Ishtiaq, F., Graves, G. R., Olson, S. L., Gering, E., Peirce, M. A., Milensky, C. M., Schmidt, B. K., Gebhard, C. and Fleischer, R. C. (2006). Avian haematozoa in South America: a comparison of temperate and tropical zones. Ornithological Monographs 60, 98–111.Google Scholar
Felsenstein, J. (1985). Confidence intervals on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.Google Scholar
Harris, D. J., Maia, J. P. and Perera, A. (2011). Molecular characterization of Hepatozoon species in reptiles from the Seychelles. Journal of Parasitology 97, 106–110. doi: 10.1645/GE-2470.1.Google Scholar
Hoare, C. A. (1932). On protozoal blood parasites collected in Uganda. With an account of the life cycle of the crocodile haemogregarine. Parasitology 24, 210–224. doi: 10.1017/S0031182000020564.Google Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MrBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.Google Scholar
Humair, P. F., Douet, V., Cadenas, F. M., Schouls, L. M., Van De Pol, I. and Gern, L. (2007). Molecular identification of bloodmeal source in Ixodes ricinus ticks using 12S rDNA as a genetic marker. Journal of Medical Entomology 44, 869–880. doi: 10.1603/0022-2585(2007)44[869:MIOBSI]2.0.CO;2.CrossRefGoogle ScholarPubMed
Hussein, A. N. (2006). Light and transmission electron microscopic studies of a haemogregarine in naturally infected fan-footed gecko (Ptyodactylus hasselquistii). Parasitology Research 98, 468–471. doi: 10.1007/s00436-005-0084-9.Google Scholar
Jarvi, S. I., Schultz, J. J. and Atkinson, C. T. (2002). PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. Journal of Parasitology 88, 153–158. doi: 10.1645/0022-3395(2002)088[0153:PDUTPO]2.0.CO;2.Google Scholar
Karbowiak, G., Rychlik, L., Nowakowski, W. and Wita, I. (2005). Natural infections of small mammals with blood parasites on the borderland of boreal and temperate forest zones. Acta Theriologica 50, 31–42. doi: 10.1007/BF03192616.CrossRefGoogle Scholar
Karbowiak, G., Stanko, M., Fričová, J., Wita, I., Hapunik, J. and Peťko, B. (2009). Blood parasites of the striped field mouse Apodemus agrarius and their morphological characteristics. Biologia 64, 1219–1224. doi: 10.2478/s11756-009-0195-3.Google Scholar
Karbowiak, G., Fričová, J., Stanko, M., Hapunik, J. and Varfalvyová, D. (2010). Blood parasites of mound-building mouse, Mus spicilegus Petényi, 1882 (Mammalia, Rodentia). Wiadomoości Parazytologiczne 56, 63–65.Google Scholar
Laakkonen, J., Sukura, A., Oksanen, A., Henttonen, H. and Soveri, T. (2001). Haemogregarines of the genus Hepatozoon (Apicomplexa: Adeleina) in rodents from northern Europe. Folia Parasitologica 48, 263–267.Google Scholar
Labbé, A. (1894). Recherches zoologique et biologiques sur les parasites endoglobulaires du sang des Vertébrés. Archives de Zoologie Experimentale et Generale 2, 55–252.Google Scholar
Landau, I., Chabaud, A. G., Michel, J. C. and Brygoo, E. R. (1970). Mise en évidence d'un double mode de transmission chez un Hepatozoon de Reptiles malgaches. Comptes Rendus de l´Académie des Sciences 270, 2308–2310.Google Scholar
Laveran, C. L. A. (1902). Sur quelques hémogrégarines des ophidiens. Comptes Rendus Hebdomadaires des Seances de l´Académie des Sciences 135, 1036–1040.Google Scholar
Levine, N. D. (1988). The Protozoan Phylum Apicomplexa, 2nd Edn. CRC Press, Boca Raton, FL, USA.Google Scholar
Lewin, J. and Grabda-Kazubska, B. (1997). Parasites of Vipera berus L. in Poland. Acta Parasitologica, 42, 92–96.Google Scholar
Maia, J. P., Harris, D. J. and Perera, A. (2011). Molecular survey of Hepatozoon species in lizards from North Africa. Journal of Parasitology 97, 513–517. doi: 10.1645/GE-2666.1.CrossRefGoogle ScholarPubMed
Maia, J. P., Perera, A. and Harris, D. J. (2012). Molecular survey and microscopic examination of Hepatozoon Miller, 1908 (Apicomplexa: Adeleorina) in lacertid lizards from western Mediterranean. Folia Parasitologica 59, 241–248.CrossRefGoogle ScholarPubMed
Martin, J. and Lopez, P. (1999) An experimental test of the costs of antipredatory refuge use in the wall lizard, Podarcis muralis . Oikos 84, 499–505.Google Scholar
Murata, T., Inoue, M., Tateyama, S., Taura, Y. and Nakama, S. (1993). Vertical transmission of Hepatozoon canis in dogs. Journal of Veterinary Medical Science 55, 867–868.Google Scholar
Oppliger, A., Clobert, J., Lecomte, J., Lorenzon, P., Boudjemadi, K. and John-Alder, H. B. (1998). Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara . Ecology Letters 1, 129–138. doi: 10.1046/j.1461-0248.1998.00028.x.CrossRefGoogle Scholar
Paterson, W. B. and Desser, S. S. (1976). Observations of Haemogregarina balli sp. n. from the common snapping turtle, Chelydra serpentina . Journal of Eukaryotic Microbiology 23, 294–301. doi: 10.1111/j.1550-7408.1976.tb03775.x.Google 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, 870–876. doi: 10.1645/0022-3395(2001)087[0870:PONSSR]2.0.CO;2.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818. doi: 10.1093/bioinformatics/14.9.817.Google Scholar
Ramdan, N. F., Saoud, M. F. A., Mohammed, S. H. and Fawzi, S. M. (1996). On a new haemogregarine of Varanus griseus from Egypt. Qatar University Science Journal 16, 119–125.Google Scholar
Richards, F. A., Sehgal, R. N. M., Jones, H. I. and Smith, T. B. (2002). A comparative analysis of PCR-based detection methods for avian malaria. Journal of Parasitology 88, 819–822. doi: 10.1645/0022-3395(2002)088[0819:ACAOPB]2.0.CO;2.Google Scholar
Robin, L. A. (1936). Cycle évolutif d'un Hepatozoon de Gecko verticillatus . Annales de l´Institut Pasteur (Paris) 56, 376–394.Google Scholar
Sambon, L. W. and Seligman, C. G. (1907). Descriptions of five new species of haemogregarines from snakes. Proceedings of the Zoological Society of London 19, 283–284.Google Scholar
Saoud, M. F. A., Ramdan, N. F., Mohammed, S. H. and Fawzi, A. M. (1995). Haemogregarines of geckos in Egypt, together with a description of Haemogregarina helmymohammedi n. sp. Qatar University Science Journal 15, 131–146.Google Scholar
Saoud, M. F. A., Ramdan, N. F., Mohammed, S. H. and Fawzi, A. M. (1996). On two new haemogregarines (Protozoa: Apicomplexa) from colubrid and elapidae snakes in Egypt. Qatar University Science Journal 16, 127–139.Google Scholar
Shanavas, R. K. and Ramachandran, P. (1990). Life history of Hepatozoon octosporei sp. n., a new Haemogregarine from the Skink, Mabuya carinata (Schneider), with notes on the in vitro excystment of its oocysts. Archive für Protistenkunde 138, 127–137. doi: 10.1016/S0003-9365(11)80154-5.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, 1189–1198. doi: 10.1645/GE-1200R.1.Google Scholar
Sloboda, M., Kamler, M., Bulantová, J., Votýpka, J. and Modrý, D. (2008). Rodents as intermediate hosts of Hepatozoon ayorgbor (Apicomplexa: Adeleina: Hepatozoidae) from the African ball python, Python regius? Folia Parasitologica 55, 13–16. doi: 10.1645/GE-1200R.1.Google Scholar
Smith, T. G. (1996). The genus Hepatozoon (Apicomplexa: Adeleina). Journal of Parasitology 82, 565–585.Google Scholar
Smith, T. G., Desser, S. S. and Martin, D. S. (1994). The development of Hepatozoon sipedon (Apicomplexa: Adeleina: Hepatozoidae) in its natural host, the Northern water snake (Nerodia sipedon sipedon), the culicine vectors, Culex pipiens and Culex territans, and an intermediate host, the Northern leopard frog (Rana pipiens). Parasitology Research 80, 559–568. doi: 10.1007/BF00933003.Google Scholar
Swofford, D. L. (2002). PAUP. Phylogenetic Analysis Using Parsimony. Version 4. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Telford, S. R. Jr. (1984). Interpopulation variation of a saurian malaria, Plasmodium sasai Telford & Ball, 1969, in three host species distributed within a range of 24° north latitude. International Journal for Parasitology 12, 17–22. doi: 10.1016/0020-7519(82)90089-3.Google Scholar
Telford, S. R. Jr. (2009). Hemoparasites of Reptilia, Color Atlas and Text, 1st Edn. CRC Press, Boca Raton, FL, USA.Google Scholar
Telford, S. R. Jr. (2010). Three new Hepatozoon species (Apicomplexa: Hepatozoidae) infecting the florida kingsnake, Lampropeltis getula floridana . Journal of Parasitology 96, 162–169. doi: 10.1645/GE-2161.1.CrossRefGoogle ScholarPubMed
Telford, S. R. Jr., 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, 890–905. doi: 10.1645/0022-3395(2001)087[0890:HSITCO]2.0.CO;2.Google Scholar
Telford, S. R. Jr., Moler, P. E. and Butler, J. F. (2008). Hepatozoon species of the timber rattlesnake in northern Florida: evidence of salivary gland oocysts and a natural cross-familial transmission of an Hepatozoon species. Journal of Parasitology 94, 520–523. doi: 10.1645/GE-1330.1.Google Scholar
Telford, S. R., Moler, P. E. and Butler, J. F. (2012). Four additional Hepatozoon species (Apicomplexa: Hepatozoidae) from north Florida ratsnakes, genus Pantherophis . Folia Parasitologica 59, 167–172. doi: 10.1645/GE-2161.1.Google Scholar
Thiroux, A. (1910). Une hémogrégarine de Crocodilus niloticus . Comptes Rendus de la Societé de Biologie 69, 577–578.Google Scholar
Tomé, B., Maia, J. P. and Harris, D. J. (2012). Hepatozoon infection prevalence in four snake genera: influence of diet, prey parasitemia levels, or parasite type? Journal of Parasitology 98, 913–917. doi: 10.1645/GE-3111.1.CrossRefGoogle ScholarPubMed
Üjvári, 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, 670–672. doi: 10.1645/GE-204R.Google Scholar
Valkiūnas, G., Iezhova, T. A., Križanauskienė, A., Palinauskas, V., Sehgal, R. N. M. and Bensch, S. (2008). A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology 94, 1395–1401. doi: 10.1645/GE-1570.1.Google Scholar
Vilcins, I. M. E., Üjvári, B., Old, J. M. and Deane, E. (2009). Molecular and morphological description of Hepatozoon species in reptiles and their ticks in the Northern territory, Australia. Journal of Parasitology 95, 434–442. doi: 10.1645/GE-1725.1.Google 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 preventative zoological medicine. Journal of Zoo and Wildlife Medicine 25, 538–547.Google Scholar