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First report of Hepatozoon (Apicomplexa: Adeleorina) from king ratsnakes (Elaphe carinata) in Shanghai, with description of a new species

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Abstract

Hepatozoon species are the most common hemoparasites of snakes. In this study, Hepatozoon parasites were examined for the first time in king rat snakes (Elaphe carinata) from Shanghai, China. All 10 snakes were found to be infected with Hepatozoon gamonts. The gamonts were folded back in a hook-wise fashion for about 3 μm at one end. Parasitemia levels ranged from 4–43 infected erythrocytes per 1,000 examined. The gamonts changed the morphology of the parasitized erythrocytes. Although the gamonts showed some distinct variations in both the parasite and its nucleus, phylogenetic analysis indicated that all the E. carinata in this study formed a monophyletic group, and were distinct from all other published Hepatozoon species. A new species, Hepatozoon chinensis, was proposed based on the molecular and morphologic evidence.

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References

  • Allen K.E., Yabsley M.J., Johnson E.M., Reichard M.V., Panciera R.J., Ewing S.A., Little S.E. 2011. Novel Hepatozoon in vertebrates from the southern United States. Journal of Parasitology, 97, 648–653. DOI: 10.1645/GE-2672.1

    Article  Google Scholar 

  • Barta J.R., Ogedengbe J.D., Martin D.S., 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, 71–180. DOI: 10.1111/j.1550-7408.2011.00607.x

    Article  Google Scholar 

  • Borner C. 1901. Untersuchungen uber Hamosporidien. I. Ein Beitrag zur Kenntnis des genus Haemogregarina Danilewsky. Z Wissenscbaft Zool., 69, 398–416

    Google Scholar 

  • Brown G.P., Shilton C.M., Shine R. 2006. Do parasites matter? Assessing the fitness consequences of haemogregarine infection in snakes. Canadian Journal of Zoology, 84, 668–676. DOI: 10.1139/z06-044

    Article  Google Scholar 

  • Carreno R.A., Martin D.S., 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. DOI: 10.1007/s004360050 655

    Article  CAS  Google Scholar 

  • Criado-Fornelio A., Buling A., Casado N., Cimenez C., Ruas J., Wendt L., da Rosa-Faria N., Pinheiro M., Rey-Valeiron C., 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

    Article  CAS  Google Scholar 

  • Criado-Fornelio A., Buling A., Pingret J.L., Etievant M., Boucraut-Baralon C., Alongi A., Agnone A., Torina A. 2009. Hemoprotozoa of domestic animals in France: Prevalence and molecular characterization. Parasitology Research, 159, 73–76. DOI: 10.1016/j.vetpar.2008.10.012

    CAS  Google Scholar 

  • Criado-Fornelio A., Ruas J.L., Casado N., Farias N.A.R., Soares M.P., Muller G., Brum J.G.W., Berne M.E.A., Buling-Sarana A., 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

    Article  CAS  Google Scholar 

  • Garnham P.C.C. 1950. Blood parasites of East African vertebrates, with a brief description of exo-erythrocytic schizogony in Plasmodium pitmani. Parasitology, 40, 328–336. DOI: 10.1017/S0031182000018205

    Article  CAS  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

    CAS  Google Scholar 

  • Harris D.J., Damas-Moreira I., Maia J.P.M.C., Perera A. 2014. First report of Hepatozoon (Apicomplexa: Adeleorina) in Caecilians, with description of a new species. Journal of Parasitology, 100, 117–120. DOI:10.1645/13-203.1

    Article  Google Scholar 

  • Harris D.J., Maia J.P.M.C., 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

    Article  Google Scholar 

  • Huelsenbeck J.P., Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755. DOI: 10.1093/bioinformatics/17.8.754.

    Article  CAS  Google Scholar 

  • Jacobson E.R. (Ed.) 2007. Infectious diseases and pathology of Reptiles: Color atlas and text. CRC Press: Taylor and Francis group, Boca Raton, Florida, 736 pp.

    Book  Google Scholar 

  • Kim B.J., Smith T.G., Desser S.S. 1998. The life history and host specificity of Hepatozoon clamatae (Apicomplexa: Adeleoria) and ITS-1 nucleotide sequence variation of Hepatozoon species of frogs and mosquitoes from Ontario. Journal of Parasitology, 84, 789–797. DOI: 10.2307/3284589

    Article  CAS  Google Scholar 

  • Kubo M., Uni S., Agatsuma T., Nagataki M., Panciera R.J., Tsubota T., Nakamura S., Sakai H., Masegi T., Yanai T. 2008. Hepatozoon ursi n. sp. (Apicomplexa: Hepatozoidae) in Japanese black bear (Ursus thibetanus japonicus). Parasitology International, 57, 287–294. DOI: 10.1016/j.parint.2008.01.002

    Article  Google Scholar 

  • Levine N.D. (Ed.) 1988. The protozoan phylum Apicomplexa. CRC Press, Boca Raton, Florida, 224 pp.

    Google Scholar 

  • Li D.S. 1987. Description of Hepatozoon guangdongense sp. nov. (Eucoccodia: Haemogregarinidae). Acta Zootaxonomica Sinica, 12, 113–118

    Google Scholar 

  • Madsen T., Ujvari B., Olsson M. 2005. Old pythons stay fit; effects of haematozoan infections on life history traits of a large tropical predator. Oecologia, 142, 407–412. DOI: 10.1007/s00 442-004-1742-9

    Article  Google Scholar 

  • Maia J.P.M.C., Harris D.J., 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

    Article  Google Scholar 

  • Maia, J.P.M.C., Perera A., Harris D.J. 2012. Molecular survey and microscopic examination of Hepatozoon Miller, 1908 (Apicomplexa: Adeleorina) in lacertid lizards from the western Mediterranean. Folia Parasitologica, 59, 241–248. DOI: 10.14411/fp.2012.033

    Article  Google Scholar 

  • Merino S., Vasquez R.A., Martinez J., Celis-Diez J.L., Gutierrez-Jimenez L., Ippi S., Sanchez-Monsalvez I., Martinez-de la Puente J. 2009. Molecular characterization of an ancient Hepatozoon species parasitizing the ‘living fossil’ marsupial ‘Monito del Monte’ Dromiciops gliroides from Chile. Biological Journal of the Linnean Society, 98, 568–576. DOI: 10.1111/j.1095-8312.2009.01302.x

    Article  Google Scholar 

  • Moco T.C., da Silva R.J., Madeira N.G., dos Santos Paduan K., Rubini A.S., Leal D.D.M., O’Dwyer L. H. 2012. Morphological, morphometric, and molecular characterization of Hepatozoon spp. (Apicomplexa: Hepatozoidae) from naturally infected Caudisona durissa terrifica (Serpentes: Viperidae). Parasitology Research, 110, 1393–1401. DOI: 10.1007/s00436-011-2639-2

    Article  Google Scholar 

  • Moco T.C., O’Dwyer L.H., Vilela F.C., Barrella T.H., da Silva D.J. 2002. Morphologic and morphometric analysis of Hepatozoon spp. (Apicomplexa: Hepatozoidae) of snakes. Memórias do Instituto Oswaldo Cruz, 97, 1169–1176. DOI: 10.1590/S0074-02762002000800019

    Article  Google Scholar 

  • O’Dwyer L.H., Moco T.C., Paduan K.S., dos Santos Paduan K., Spenassatto C., da Silva R.J., Ribolla P.E.M. 2013. Description of three new species of Hepatozoon (Apicomplexa, Hepatozoidae) from Rattlesnakes (Crotalus durissus terrificus) based on molecular, morphometric and morphologic characters. Experimental Parasitology, 135, 200–207. DOI: 10.1016/j.exppara. 2013.06.019

    Article  Google Scholar 

  • Oyamada M., Davoust B., Boni M., Dereure J., Bucheton B., Hammad A., Itamoto K., Okuda M., Inokuma H. 2005. Detection of Babesia canis rossi, B. canis vogeli, and Hepatozoon canis in dogs in a village of eastern Sudan by using a screening PCR and sequencing methodologies. Clinical and Diagnostic Laboratory Immunology, 12, 1343–1346. DOI: 10.1128/CDLI.12. 11.1343-1346.2005

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pedersen A.B., Jones K.E., Nunn C.L., Altizer S. 2007. Infectious diseases and extinction risk in wild animals. Conservation Biology, 21, 1269–1279. DOI: 10.1111/j.1523-1739.2007.00776.x

    Article  Google Scholar 

  • Perkins S.L., 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:PONS SR]2.0.CO;2

    Article  CAS  Google Scholar 

  • Pessoa S.B., De Biasi P. 1973. Consideracoes taxonomicas sobre cistos esquizogonicose sobre gametocitos de Hepatozoon (Sporozoa, haemogregarinidae) parasitas de serpents brasileiras. Memórias do Instituto Butantan, 37, 291–298

    Google Scholar 

  • Posada D., Crandall K.A. 1998. Modeltest: Testing the model of DNA substitution. Bioinformatics, 14, 817–818. DOI: 10.1093/bioinformatics/14.9.817

    Article  CAS  Google Scholar 

  • Rubini A.S., dos Santos Paduan K., Lopes V.V.A., O’Dwyer L.H. 2008. Molecular and parasitological survey of Hepatozoon canis (Apicomplexa: Hepatozoidae) in dogs from rural area of Sao Paulo state, Brazil. Parasitology Research, 102, 895–899. DOI: 10.1007/s00436-007-0846-7

    Article  Google Scholar 

  • Sloboda M., Kamler M., Bulantova J., Votypka J., Modry 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

    Article  CAS  Google Scholar 

  • Smith T.G. 1996. The genus Hepatozoon (Apicomplexa: Adeleina). Journal of Parasitology, 84, 565–585.

    Article  Google Scholar 

  • Smith T.G, Kim B., Desser S.S. 1999. Phylogenetic relationships among Hepatozoon species from snakes, frogs and mosquitoes of Ontario, Canada, determined by ITS-1 nucleotide sequences and life-cycle, morphological and developmental characteristics. International Journal for Parasitology, 29, 293–304. DOI: 10.1016/S0020-7519(98)00198-2.

    Article  CAS  Google Scholar 

  • Swofford D.L. 2002. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.10. Sinauer Associates, Sunderland, Mass

    Google Scholar 

  • Telford S.R. Jr. 1984. Haemoparasites of reptiles. In: (Eds. G.L. Hoff, Frye F.L. and E.R. Jacobson) Diseases of amphibians and reptiles. Plenum Press, New York, 385–517

    Chapter  Google Scholar 

  • Telford S.R. Jr. (Ed.). 2009. Hemoparasites of the Reptilia: Color atlas and text. CRC Press, Taylor and Francis Group, Boca Raton, Florida, 394 pp.

    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

    Article  Google Scholar 

  • Telford S.R. Jr., Butler J.F., Telford R.S. 2002. Hepatozoon species (Apicomplexa: Hepatozoidae) of the corn snake, Elaphe guttata (Serpentes: Colubridae) and the pigmy rattlesnake, Sistrurus miliarius barbouri (Serpentes: Viperidae) in south Florida. Journal of Parasitology, 88, 778–782. DOI: 10.1645/0022-3395 (2002)088[0778:HSAHOT]2.0.CO;2

    Article  Google Scholar 

  • Telford S.R. Jr., Moler P.E., Butler J.F. 2008. Hepatozoon species of the timber rattlesnake in Northern Florida: description of a new species, evidence of salivary gland oocysts, and a natural cross-familial transmission of a Hepatozoon species. Journal of Parasitology, 94: 520–523. DOI: 10.1645/GE-1330.1

    Article  Google Scholar 

  • Telford S.R. Jr., Ernst J.A., Clark A.M., Butler J.F. 2004. Hepatozoon sauritus: A polytopic hemogregarine of three genera and four species of snakes in North Florida, with specific identity verified from genome analysis. Journal of Parasitology, 90, 352–358. DOI: 10.1645/GE-3258

    Article  Google Scholar 

  • Telford S.R. Jr., Wozniak E.J., 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:HSIT CO]2.0.CO;2

    Article  Google Scholar 

  • Tome B., Maia J.P.M.C., Harris D.J. 2013. Molecular assessment of apicomplexan parasites in the snake Psammophis from North Africa: do multiple parasite lineages reflect the final vertebrate host diet? Journal of Parasitology, 99, 883–887. DOI: 10.1645/12-95.1

    Article  Google Scholar 

  • Ujvari B., Madsen T., 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: 10.1645/12-95.1

    Article  Google Scholar 

  • Vilcins I.M.E., Ujvari B., Old J.M., Deane E. 2009. Molecular and morphological description of a Hepatozoon species in reptiles and their ticks in the Northern Territory, Australia. Journal of Parasitology, 95, 434–442. DOI: 10.1645/GE-1725.1

    Article  CAS  Google Scholar 

  • Wozniak E.J., Kazacos K.R., Telford S.R.Jr., Mclaughlin G.L. 1996. Characterization of the clinical and anatomical pathological changes associated with Hepatozoon mocassini infections in unnatural reptilian hosts. International Journal for Parasitology, 26, 141–146. DOI: 10.1016/0020-7519(95)00110-7

    Article  CAS  Google Scholar 

  • Wozniak E.J., Telford S.R.Jr., 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 

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  1. Hongyu Han and Youling Wu equally contributed to this paper and should be considered as co-first authors

Authors and Affiliations

  1. Key Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Science, No. 518 Ziyue Road, Minhang District, Shanghai, 200241, China

    Hongyu Han, Youling Wu, Hui Dong, Shunhai Zhu, Liujia Li, Qiping Zhao, Yange Wang & Bing Huang

  2. Department of Wildlife Protection Administration, Shanghai, 200233, China

    Di Wu & Enle Pei

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  1. Hongyu Han
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  2. Youling Wu
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  3. Hui Dong
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  4. Shunhai Zhu
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  10. Bing Huang
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Correspondence to Bing Huang.

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Han, H., Wu, Y., Dong, H. et al. First report of Hepatozoon (Apicomplexa: Adeleorina) from king ratsnakes (Elaphe carinata) in Shanghai, with description of a new species. Acta Parasit. 60, 266–274 (2015). https://doi.org/10.1515/ap-2015-0038

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