Skip to main content
Log in

Molecular characterization and identification of Hepatozoon species Miller, 1908 (Apicomplexa: Adeleina: Hepatozoidae) in captive snakes from Brazil

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Species of Hepatozoon are parasites frequently recorded in snakes. The species identification of this genus was based mostly on the gametocyte morphology and morphometric calculations. For more reliable results, molecular characterization, an initial step for the correct identification of Hepatozoon species, has been used. This study aimed to determine the prevalence and identification of Hepatozoon species in captive snakes from Brazil. To that end, morphological, morphometric, and molecular data were obtained. A total of 157 snakes; 128 venomous (Crotalus durissus) and 29 non-venomous (Epicrates crassus and Boa constrictor) were screened for Hepatozoon blood parasites. Using light microscopy, 20 (12.78%) snakes were found positive for Hepatozoon spp., of which 6/29 (20.7%) were non-venomous and 14/128 (10.9%) were venomous; all with low parasitemia. Polymerase chain reaction (PCR), performed with the primers HepF300/Hep900, confirmed all 20 (100%) samples positive for hemogregarines. Species of Hepatozoon were identified from eight sequenced samples. Two previously described species, Hepatozoon cuestensis and Hepatozoon musa, were identified. The present study is the first to report H. musa within the snake hosts E. crassus and C. durrisus. In addition, a potentially new Hepatozoon species from B. constrictor was identified.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ball GH, Chao J, Telford SR Jr (1967) The life history of Hepatozoon rarefaciens (Sambon and Seligmann, 1907) from Drymarchon corais (Colubridae), and its experimental transfer to constrictor constrictor (Boidae). J Parasitol 53:897–909

    Article  CAS  Google Scholar 

  • Ball GH, Chao J, Telford SR Jr (1969) Hepatozoon fusifex sp. n., a haemogregarine from Boa constrictor producing marked morphological changes in infected erythrocytes. J Parasitol 55:800–813

    Article  CAS  Google Scholar 

  • Barta JR (2000) Suborder Adeleorina Léger, 1911. In: Lee JJ, Leesdale GF, Bradbury P (eds) The illustrated guide to the protozoa, 2nd edn. Allen Press, Lawrence, pp 305–318

    Google Scholar 

  • Borges-Nojosa DM, Borges-Leite MJ, Maia JP, Zanchi-Silva D, Braga RR, Harris DJ (2017) A new species of Hepatozoon Miller, 1908 (Apicomplexa: Adeleina) from the snake Philodryas nattereri Steindacher (Squamata: Dipsadidae) in northeastern Brazil. Syst Parasitol 94:65–72

    Article  Google Scholar 

  • Carini A (1947) Contribuição ao estudo das hemogregarinas de serpentes da família Boídeos. Arq Biol 31:61–63

    Google Scholar 

  • Caudell JN, Whittier J, Conover MR (2002) The effects of haemogregarine-like parasites on brown tree snakes (Boiga irregularis) and slates-grey snakes (Stegonotus cucullatus) in Queensland, Australia. Int Biodeter Biodegrad 49:113–119

    Article  Google Scholar 

  • Cook CA, Lawton SP, Davies AJ, Smit NJ (2014) Reassignment of the land tortoise haemogregarine Haemogreagrina fitzsimonsi Dias 1953 (Adeleorina: Haemogregarinidae) to the genus Hepatozoon Miller 1908 (Adeleorina: Hepatozoidae) based on parasites morphology, life cycle and phylogenetic analysis of 18S rDNA sequence fragments. Parasitol 141:1611–1620

    Article  Google Scholar 

  • Cook CA, Netherlands EC, Van As J, Smit NJ (2018) Two new species of Hepatozoon (Apicomplexa: Hepatozoidae) parasiting species of Philothamnus (Ophidia: Colubridae) from South Africa. Folia Parasitol 65:4–11

    Article  Google Scholar 

  • Darriba D, Toboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and high-performance computing. Nat Methods 9:772

    Article  CAS  Google Scholar 

  • De Biasi P, Pessoa SP, Vieira ACG (1972) Nota sobre longa latência de infecção por hemogregarina em uma serpente peçonhenta: Bothrops moojeni. Atas Soc Biol 15:71–73

    Google Scholar 

  • De Biasi P, Cardoso RB Jr, Santos SMA (1989) Presença de Hepatozoon plimmeri (Sambon, 1909) -Coccidia, Haemogregarinidae - em exemplar de Bothrops jararaca (Wied, 1984) - Serpentes, Viperidae, Crotalinae - mantido em cativeiro. Mem Inst Butantan 55:117–121

    Google Scholar 

  • Desser SS (1993) The Haemogregarinidae and Lankesterellidae. Parasitol Protozo 44:247–272

    Google Scholar 

  • Eisen RJ, Schall JJ (2000) Life history of malaria parasite (Plasmodium mexicanum): independent traits and basis for variation. Proc Biol Sci 267:793–799

    Article  CAS  Google Scholar 

  • Glaser V, Boni AP, Albuquerque CAC (2008) Ocorrência de Hepatozoon spp. (Apicomplexa, Hepatozoidae) em serpentes do gênero Bothrops de cativeiro. Arq Bras Med Vet Zootec 60:1288–1290

    Article  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  Google Scholar 

  • Haklová B, Majláthová V, Majláth I, Harris DJ, Petrilla V, Litschka-Koen T, Oros M, Petko B (2013) Phylogenetic relationship of Hepatozoon blood parasites found in snakes from Africa, America and Asia. Parasitol 141:389–398

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harris DJ, Maia JP, Perera A (2011) Molecular characterization of Hepatozoon species in reptiles from the Seychelles. J Parasitol 97:106–110

    Article  Google Scholar 

  • Harris DJ, Borges-Nojosa DM, Maia JP (2015) Prevalence and diversity of Hepatozoon in native and exotic geckos from Brazil. J Parasitol 101:80–85

    Article  Google Scholar 

  • Hernandez LM, Ballou L, Ballou CE (1990) Separation of yeast asparagine-linked oligosaccharides by high-performance anion-exchange chromatography. Carbohydr Res 203:1–11

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) Mr Bayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  Google Scholar 

  • Hull RW, Camin JH (1960) Haemogregarines in snakes: the incidence and identity of the erythrocytic stages. J Parasitol 46:515–523

    Article  CAS  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond AJ (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  Google Scholar 

  • Lopes FC, Azevedo SS, Dantas LAB, Freitas CIA, Batista CSA, Azevedo AS (2010) Ocorrência de Hepatozoon ssp. (Apicomplexa, Hepatozoidae) em serpentes Boa constrictor mantidas em cativeiro no semi-árido do estado de Rio Grande do Norte. Arq Bras Med Vet Zootec 62:1285–1287. https://doi.org/10.1590/S0102-09352010000500038

    Article  Google Scholar 

  • Luz MA, Meneses AMC, Moraes CCG, Seixas LS, Lima DJS, Ruffeil LAAAS, Castro PHG, Costa AM (2012) Determinação de hemogregarina em Boa constrictor constrictor mantidas em cativeiro. Pesqui Vet Bras 32:781–785. https://doi.org/10.1590/S0100-736X2012000800017

    Article  Google Scholar 

  • Madsen T, Ujvari B, Olsson M (2005) Old phytons stay fit: effects of haematozoan infections on life history traits of a large tropical predator. Oecologia 142:407–712

    Article  Google Scholar 

  • Maia JP, Harris DJ, Perera A (2011) Molecular survey of Hepatozoon species in lizards from North Africa. J Parasitol 97:513–517

    Article  Google Scholar 

  • Mesquita PCMD, Borges-Nojosa DM, Passos DC, Bezerra CH (2011) Ecology of Philodryas nattereri (Serpentes: Dipsadidae) in the Brazilian semi-arid region. Herpetol J 21:193–198

    Google Scholar 

  • Moller AP (1997) Parasitism and the evolution of the host life history. In: Clayton DH, Moore J (eds) Host-parasite evolution: general principles and avian models. Oxford University Press, Oxford, pp 105–127

    Google Scholar 

  • Netherlands EC, Cook C, Du Preez LH, Vanhove MPM, Brendonck L, Smit NJ (2017) Monophyly of the species of Hepatozoon (Adeleorina: Hepatozoidae) parasiting (African) anurans, with the description of three new species from hyperoliid frogs in South Africa. Parasitol 4:1–12

    Google Scholar 

  • O’Dwyer LH, Moço TC, Barella TH, Vilela FC, Silva RJ (2003) Description of the gamonts of a small species of Hepatozoon sp. (Apicomplexa, Hepatozoidae) found in Crotalus durissus terrificus (Serpentes, Viperidae). Parasitol Res 92:110–112

    Article  Google Scholar 

  • O’Dwyer LH, Silva RJ, Madeira NG (2004) Description of gametogonic and sporogonic stages of Hepatozoon spp. (Apicomplexa: Hepatozoidae) from Caudisona terrifica (Serpentes, Viperidae). Parasitol. Res 108:110–112

    Article  Google Scholar 

  • O’Dwyer LH, Moço TC, Paduan KS, Spenassatto C, Silva RJ, Ribolla PEM (2013) Descriptions of three new species of Hepatozoon (Apicomplexa, Hepatozoidae) from rattlesnakes (Crotalus durissus terrificus) based on molecular, morphometric and morphologic characters. Exp Parasitol 135:200–207. https://doi.org/10.1016/j.exppara.2013.06.019

    Article  CAS  PubMed  Google Scholar 

  • O'Donoghue P (2017) Haemoprotozoa: making biological sense of molecular phylogenies. Int J Parasitol Parasites Wildl 6:241–256

    Article  Google Scholar 

  • Page RDM (1996) Treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:294–301

    Google Scholar 

  • Sambon LW, Seligmann CG (1907) Descriptions of five new species of haemogregarines from snakes. Proc Zool Soc London:283–284

  • Santos MMV, O’Dwyer LH, Silva RJ (2005) Seasonal variation of Hepatozoon spp. (Apicomplexa, Hepatozoidae) parasitemia from Boa constrictor amarali (Serpentes, Boidae) and Hydrodynastes gigas (Serpentes, Colubridae). Parasitol Res 97:94–97

    Article  Google Scholar 

  • Sawaya RJ, Marques OAV, Martins M (2008) Composição e história natural das serpentes de Cerrado de Itirapina, São Paulo, sudeste do Brasil. Biota Neotrop 8:127–148

    Article  Google Scholar 

  • Siddall ME, Burison EM (1995) The development of a hemogregarina of Lycodes raridens form Alaska in its definitive leech host. J Parasitol 80:75–569

    Google Scholar 

  • Sloboda M, Kamler M, Bulantová J, Votýpka J, Modrý D (2008) Rodents as intermediate hosts of Hepatozoon ayorgbor (Apicomplexa: Adeleina: Hepatozoidae) from the African ball python, Phython regius? Folia Parasitol 55:13–16

    Article  CAS  Google Scholar 

  • Smith TG (1996) The genus Hepatozoon (Apicomplexa: Adeleina). J Parasitol 82:565–585

    Article  CAS  Google Scholar 

  • Smith TG, Desser SS, Martin DS (1994) The development of Hepatozoon sipedon sp. nov. (Apicomplexa: Adeleina: Hepatozoidae) in its natural host, the northern water snake (Nerodia sipedon sipedon), in the culicine vectors Culex pipiens and C. territans, and in an intermediate host, the northern leopard frog (Rana pipiens). Parasitol Res 80:559–568

    Article  CAS  Google Scholar 

  • Teldord SR Jr (2010) Three new Hepatozoon species (Apicomplexa: Hepatozoidae) infecting the Florida kingsnakes, Lampropeltis getula floridana. J Parasitol 96:162–169

    Article  Google Scholar 

  • Telford SR (1984) Reptilian hemoparasites. In: Hoff GL, Frye FL, Jacobson ER (eds) Diseases of amphibians and reptiles. Plenum Publishing Corporation, New York, pp 385–517

    Chapter  Google Scholar 

  • Telford SR Jr (2005) Haemocystidium species from the east African gecko Lygodactylus capensis grotei. J Parasitol 91:135–138

    Article  Google Scholar 

  • Telford SR Jr (2009) Hemoparasites of the reptilian: color atlas and text. CRC Press, Boca Raton

    Google Scholar 

  • Telford SR Jr, Ernst JA, Clark AM, Butler JF (2004) Hepatozoon sauritus: a polytopic hemogregarine of three genera and four species of snakes in north Florida, with specific identity verified from genome analysis. J Parasitol 90:352–358

    Article  Google Scholar 

  • Thrall MA, Baker DC, Campbell TW, De Nicola D, Fettman MJ, Lassend ED, Rebar A, Weiser G (2007) Hematologia e Bioquímica Clínica e Veterinária, 2nd edn. Roca, São Paulo, p 26

  • Tomé B, Maia JP, Harris DJ (2012) Hepatozoon infection prevalence in four snake genera: influence of diet, prey parasitemia levels, or parasite type? J Parasitol 98:913–917

    Article  Google Scholar 

  • Uetz P (2016) The reptile database. Herpetol Rev 47:330–334

    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. J Parasitol 90:670–672

    Article  Google Scholar 

  • Vitt LJ (1980) Ecological observations on sympatric Philodryas (Colubridae) in northeastern Brazil. Pap Avulsos de Zool 34:87–98

    Google Scholar 

  • Wozniak EJ (1998) Granulomatous hepatitis associated with Hepatozoon sp. meronts in a southern water snake (Nerodia fasciata pictiventris). J Zoo Wildl Med 29:68–71

    CAS  PubMed  Google Scholar 

  • Zippel KC, Lillywhite HB, Mladinich CR (2001) New vascular system in reptiles: anatomy and postural hemodynamics of the vertebral venous plexus in snakes. J Morphol 250:173–184

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Vera Lúcia Brites and the team of Reptile sector, as well as the team of LAPAS, for the help provided in blood collection of snakes. We thank Guilherme Carrara Moreira Paiva and Daniela Ferreira Benevides for the help provided with examination of the blood extensions.

Funding

This study was financially supported by the CAPES (Improvement Coordination of Higher Education Personnel) and FAPEMIG (Foundation Research of Minas Gerais).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Letícia Pereira Úngari.

Additional information

Section Editor: Leonhard Schnittger

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Úngari, L.P., Santos, A.L.Q., O’Dwyer, L.H. et al. Molecular characterization and identification of Hepatozoon species Miller, 1908 (Apicomplexa: Adeleina: Hepatozoidae) in captive snakes from Brazil. Parasitol Res 117, 3857–3865 (2018). https://doi.org/10.1007/s00436-018-6092-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-018-6092-3

Keywords

Navigation