Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-06-01T00:35:11.334Z Has data issue: false hasContentIssue false
  • English
  • Français

A 50-year-old redescription: molecular and morphometric characterization of Hepatozoon carinicauda Pessôa and Cavalheiro, 1969 in the brown-banded water snake Helicops angulatus (Linnaeus, 1758)

Published online by Cambridge University Press:  03 August 2022

Fabiane R. de Paula Open the ORCID record for Fabiane R. de Paula [Opens in a new window] ,
Amanda M. Picelli Open the ORCID record for Amanda M. Picelli [Opens in a new window] ,
Lívia Perles ,
Marcos R. André  and
Lúcio A. Viana Open the ORCID record for Lúcio A. Viana [Opens in a new window]
Fabiane R. de Paula*
Affiliation:
Programa de Pós-Graduação em Biodiversidade Tropical, Universidade Federal do Amapá (UNIFAP), Macapá, AP, Brazil Laboratório de Estudos Morfofisiológicos e Parasitários, Departamento de Ciências Biológicas e da Saúde, UNIFAP, Macapá, AP, Brazil
Amanda M. Picelli
Affiliation:
Fundação Oswaldo Cruz – Fiocruz Rondônia, Porto Velho, RO, Brazil Programa de Pós-Graduação em Biologia Experimental, Universidade Federal de Rondônia, Porto Velho, RO, Brazil
Lívia Perles
Affiliation:
Laboratório de Imunoparasitologia, Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista (FCAV/UNESP), Jaboticabal, SP, Brazil
Marcos R. André
Affiliation:
Laboratório de Imunoparasitologia, Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista (FCAV/UNESP), Jaboticabal, SP, Brazil
Lúcio A. Viana
Affiliation:
Programa de Pós-Graduação em Biodiversidade Tropical, Universidade Federal do Amapá (UNIFAP), Macapá, AP, Brazil Laboratório de Estudos Morfofisiológicos e Parasitários, Departamento de Ciências Biológicas e da Saúde, UNIFAP, Macapá, AP, Brazil
*
Author for correspondence: Fabiane R. de Paula, E-mail: fabianerp.ap@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The combined use of molecular and microscopic techniques has become an increasingly common and efficient practice for the taxonomic and evolutionary understanding of single-celled parasites such as haemogregarines. Based on this integrative approach, we characterized Hepatozoon found in Helicops angulatus snakes from the Eastern Amazonia, Brazil. The gamonts observed caused cell hypertrophy and were extremely elongated and, in some cases, piriform (mean dimensions: 25.3 ± 1.9 × 8.6 ± 1.3 μm). These morphological features correspond to Hepatozoon carinicauda, described 50 years ago in the snake Helicops carinicaudus in the southeast region of Brazil. Phylogenetic and genetic divergence analyses, performed with the sequence obtained from the amplification of a 590 bp fragment of the 18S rRNA gene, revealed that Hepatozoon in He. angulatus differed from the other lineages retrieved from GenBank, and was clustered singly in both the phylogenetic tree and the haplotype network. The integration of these data allowed the identification of H. carinicauda in a new aquatic host, and increased the knowledge of its geographical distribution. Therefore, the present study included the first redescription of a Hepatozoon species in a snake from the Brazilian Amazon.

Keywords

Haemogregarinesmolecular descriptionneotropical snakestaxonomy18S rRNA
Type
Research Article
Information
Parasitology , Volume 149 , Issue 11 , September 2022 , pp. 1468 - 1478
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

Abdel-Baki, AA, Al-Quraishy, S and Zhang, J (2014) Redescription of Haemogregarina garnhami (Apicomplexa: Adeleorina) from the blood of Psammophis schokari (Serpentes: Colubridae) as Hepatozoon garnhami n. comb. based on molecular, morphometric and morphologic characters. Acta Parasitologica 59, 294–300.CrossRefGoogle ScholarPubMed
Aguiar, LFS and Di-Bernardo, M (2004) Diet and feeding behavior of Helicops infrataeniatus (Serpentes: Colubridae: Xenodontinae) in southern Brazil. Studies on Neotropical Fauna and Environment 39, 7–14.CrossRefGoogle Scholar
Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Ávila, RW, Ferreira, VL and Arruda, JA (2006) Natural history of the South American water snake Helicops leopardinus (Colubridae: Hydropsini) in the Pantanal, central Brazil. Journal of Herpetology 40, 274–279.CrossRefGoogle Scholar
Bandelt, H, Forster, P and Rohl, A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Barta, JR, Ogedengbe, JD, Martin, DS and Smith, TG (2012) Phylogenetic position of the adeleorinid coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) inferred using 18S rRNA sequences. Journal of Eukaryotic Microbiology 59, 171–180.CrossRefGoogle Scholar
Borges-Nojosa, DM, Borges-Leite, MJ, Maia, JP, Zanchi-Silva, D, da Rocha, BR and Harris, DJ (2017) A new species of Hepatozoon Miller, 1908 (Apicomplexa: Adelerina) from the snake Philodryas nattereri Steindachner (Squamata: Dipsadidae) in northeastern Brazil. Systematic Parasitology 94, 65–72.CrossRefGoogle Scholar
Bouer, A, André, MR, Gonçalves, LR, Luzzi, MDC, Oliveira, JPD, Rodrigues, AC, Varani, AM, Miranda, VFO, Perles, L, Werther, K and Machado, RZ (2017) Hepatozoon caimani in Caiman crocodilus yacare (Crocodylia Alligatoridae) from North Pantanal, Brazil. Brazilian Journal of Veterinary Parasitology 26, 352–358.Google Scholar
Braz, HB, Scartozzoni, RR and Almeida-Santos, SM (2016) Reproductive modes of the South American water snakes: a study system for the evolution of viviparity in squamate reptiles. Zoologischer Anzeiger 263, 33–44.CrossRefGoogle Scholar
Carvalho, TC, De Assis Montag, LF and Dos Santos-Costa, MC (2017) Diet composition and foraging habitat use by three species of water snakes, Helicops Wagler 1830 (Serpentes: Dipsadidae) in eastern Brazilian Amazonia. Journal of Herpetology 51, 215–222.Google Scholar
Cook, CA, Netherlands, EC, Smit, NJ and Van As, J (2018) Two new species of Hepatozoon (Apicomplexa; Hepatozoidae) parasitising species of Philothamnus (Ophidia: Colubridae) from South Africa. Folia Parasitologica 65, 004.CrossRefGoogle ScholarPubMed
Costa, HC and Bérnils, RS (2018) Répteis do Brasil e suas Unidades Federativas: Lista de espécies. Herpetologia Brasileira 7, 11–57.Google Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
De Paula, FR, Picelli, AM, Silva, MRL, Correa, JKC and Viana, LA (2021) Hepatozoon cevapii (Apicomplexa: Hepatozoidae) in the Thamnodynastes lanei snake (Colubridae, Tachymenini) from the Eastern Amazon, Brazil. Parasitology Research 120, 2981–2987.CrossRefGoogle ScholarPubMed
Flanley, CM, Ramalho-Ortigao, M, Coutinho-Abreu, IV, Mukbel, R, Hanafi, HA, El-Hossary, SS, Fawaz, EEY, Hoel, DF, Bray, AW, Stayback, G, Shoue, DA, Kamhawi, S, Karakus, M, Jaouadi, K, Yaghoobie-Ershadi, MR, Krüger, A, Amro, A, Kenawy, MA, Dokhan, MR, Warburg, A, Hamarsheh, O and McDowell, MA (2018) Population genetics analysis of Phlebotomus papatasi sand flies from Egypt and Jordan based on mitochondrial cytochrome b haplotypes. Parasites & Vectors 11, 214.CrossRefGoogle ScholarPubMed
Fonseca, MS, Bahiense, TC, Silva, AAB, Onofrio, VC, Barral, TD, Souza, BMP, Lira-da-Silva, RM, Biondi, I, Meyer, R and Portela, RW (2020) Ticks and associated pathogens from rescued wild animals in rainforest fragments of northeastern Brazil. Frontiers in Veterinary Science 7, 177.CrossRefGoogle ScholarPubMed
Freitas, MA (2003) Serpentes brasileiras. Malha de Sapo Publicações e Consultoria Ambiental. Brasil: Lauro de Freitas.Google Scholar
Godfrey, RD Jr, Fedynich, AM and Pence, DB (1987) Quantification of haematozoa in blood smears. Journal of Wildlife Diseases 23, 558–565.CrossRefGoogle Scholar
Gutiérrez-Liberato, GA, Lotta-Arévalo, IA, Rodríguez-Almonacid, CC, Vargas-Ramírez, M and Matta, NE (2021) Molecular and morphological description of the first Hepatozoon (Apicomplexa: Hepatozoidae) species infecting a neotropical turtle, with an approach to its phylogenetic relationships. Parasitology 148, 747–759.CrossRefGoogle ScholarPubMed
Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Harris, DJ, Maia, JP and Perera, A (2011) Molecular characterization of Hepatozoon species in reptiles from the Seychelles. Journal of Parasitology 97, 106–111.CrossRefGoogle ScholarPubMed
Harris, DJ, Santos, J, Rampedi, KM, Halajian, A and Xavier, R (2019) Genetic diversity of Hepatozoon (Apicomplexa) from domestic cats in South Africa, with a global reassessment of Hepatozoon felis diversity. Journal of the South African Veterinary Association 90, 1–6.CrossRefGoogle ScholarPubMed
Hay, ME, Poulin, R and Jorge, F (2020) Macroevolutionary dynamics of parasite diversification: a reality check. Journal of Evolutionary Biology 33, 1758–1769.CrossRefGoogle ScholarPubMed
Hodzic, A, Alic, A, Prasovic, S, Otranto, D, Baneth, G and Duscher, GG (2017) Hepatozoon silvestris sp. nov.: morphological and molecular characterization of a new species of Hepatozoon (Adeleorina: Hepatozoidae) from the European wild cat (Felis silvestris silvestris). Parasitology 144, 650–661.CrossRefGoogle ScholarPubMed
Hrazdilová, K, Cervená, B, Blanvillain, C, Foronda, P and Modrý, D (2021) Quest for the type species of the genus Hepatozoon – phylogenetic position of hemogregarines of rats and consequences for taxonomy. Systematics and Biodiversity 19, 1–10. doi:10.1080/14772000.2021.1903616.Google Scholar
Hull, RW and Camin, JH (1960) Haemogregarines in snakes: the incidence and identity of the erythrocytic stages. Journal of Parasitology 46, 515–523.CrossRefGoogle ScholarPubMed
Karadjian, G, Chavatte, JM and Landau, I (2015) Systematic revision of the adeleid haemogregarines, with creation of Bartazoon ng, reassignment of Hepatozoon argantis Garnham, 1954 to Hemolivia, and molecular data on Hemolivia stellata. Parasite 22, 31.CrossRefGoogle ScholarPubMed
Katoh, K, Rozewicki, J and Yamada, KD (2019) MAFFT online service: multiple sequence alignment, interactive, sequence choice and visualization. Briefings in Bioinformatics 20, 1160–1166.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Lainson, R, Paperna, I and Naiff, RD (2003) Development of Hepatozoon caimani (Carini, 1909) Pessôa, De Biasi & De Souza, 1972 in the caiman Caiman c. crocodilus, the frog Rana catesbeiana and the mosquito Culex fatigans. Memórias do Instituto Oswaldo Cruz 98, 103–113.CrossRefGoogle Scholar
Léveillé, AN, Zeldenrust, EG and Barta, JR (2021) Multilocus genotyping of sympatric Hepatozoon species infecting the blood of Ontario ranid frogs reinforces species differentiation and identifies an unnamed Hepatozoon species. Journal of Parasitology 107, 246–261.CrossRefGoogle ScholarPubMed
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
Maia, JP, Perera, A and Harris, DJ (2012) Molecular survey and microscopic examination of Hepatozoon Miller, 1908 (Apicomplexa: Adeleorina) in lacertid lizards from the western Mediterranean. Folia Parasitologica 59, 241–248.CrossRefGoogle ScholarPubMed
Maia, JP, Carranza, S and Harris, DJ (2016) Comments on the systematic revision of adeleid haemogregarines: are more data needed? Journal of Parasitology 102, 549–552.CrossRefGoogle ScholarPubMed
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE) 14, 1–8. doi:10.1109/GCE.2010.5676129.Google Scholar
Morand, S (2015) (macro-) Evolutionary ecology of parasite diversity: from determinants of parasite species richness to host diversification. International Journal Parasitology Parasites and Wildlife 4, 80–87.CrossRefGoogle ScholarPubMed
Morrison, DA (2009) Evolution of the Apicomplexa: where are we now? Trends in Parasitology 25, 375–382.CrossRefGoogle ScholarPubMed
Murphy, JC, Muñoz-Mérida, A, Auguste, RJ, Lasso-Alcala, O, Rivas, GA and Jowers, MJ (2020) Evidence for cryptic diversity in the Neotropical water snake, Helicops angulatus (Linnaeus, 1758) (Dipsadidade, Hydropsini), with comments on its ecology, facultative reproductive mode, and conservation. Amphibian & Reptile Conservation 14, 138–155.Google Scholar
Nogueira, CC, Argôlo, AJS, Arzamendia, V, Azevedo, JA, Barbo, FE, Bérnils, RS, Bolochio, BE, Borges-Martins, M, Brasil-Godinho, M, Braz, H, Buononato, MA, Cisneros-Heredia, DE, Colli, GR, Costa, HC, Franco, FL, Giraudo, A, Gonzalez, RC, Guedes, T, Hoogmoed, MS, Marques, OAV, Montingelli, GG, Passos, P, Prudente, ALC, Rivas, GA, Sanchez, PM, Serrano, FC, Silva, NJ, Strüssmann, C, Vieira-Alencar, JPS, Zaher, H, Sawaya, RJ and Martins, M (2019) Atlas of Brazilian snakes: verified point-locality maps to mitigate the Wallacean shortfall in a megadiverse snake fauna. South American Journal of Herpetology 14, 1–274.CrossRefGoogle Scholar
O'Dwyer, LH, Moço, TC, Paduan, KS, Spenassatto, C, Silva, RJ and Ribolla, PEM (2013) Descriptions 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.CrossRefGoogle ScholarPubMed
Perkins, SL, Martinsen, ES and Falk, BG (2011) Do molecules matter more than morphology? Promises and pitfalls in parasites. Parasitology 138, 1664–1674.CrossRefGoogle ScholarPubMed
Pessôa, SB and Cavalheiro, J (1969 a) Notas sobre hemogregarinas de serpentes brasileiras – VII. Revista Brasileira de Biologia 29, 351–354.Google Scholar
Pessôa, SB and Cavalheiro, J (1969 b) Notas sobre hemogregarinas de serpentes Brasileiras. IX. Sobre a hemogregarina da Helicops carinicauda (Wied). Revista Goiana de Medicina 15, 161–168.Google Scholar
Pessôa, SB, De Biasi, P and Puorto, G (1974) Nota sobre a frequência de hemoparasitas em serpentes do Brasil. Memórias do Instituto Butantan 38, 69–118.Google Scholar
Picelli, AM, Da Silva, MRL, Ramires, AC, Da Silva, TRR, Pessoa, FAC, Viana, LA and Kaefer, IL (2020) Redescription of Hepatozoon ameivae (Carini and Rudolph, 1912) from the lizard Ameiva ameiva (Linnaeus, 1758). Parasitology Research 119, 2659–2666.CrossRefGoogle ScholarPubMed
Poulin, R and Morand, S (2004) Parasite Biodiversity. Washington: Smithsonian Institution Press.Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Ronquist, F, Huelsenbeck, JP and Teslenko, M (2011) MrBayes 3.2 Manual: tutorials and model summaries. Available at http://mrbayes.sourceforge.net/mb3.2_manual.pdf.Google Scholar
Sanger, F, Nicklen, S and Coulson, AR (1977) DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences 74, 5463–5467.CrossRefGoogle ScholarPubMed
Schoneberg, Y and Kohler, G (2021) Distribution and identification of the species in the genus Helicops Wagler, 1830 (Serpentes, Colubridae, Xenodontinae). Arpha Preprints 10, e69234. doi:10.3897/arphapreprints.e67869.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.CrossRefGoogle ScholarPubMed
Smith, TG (1996) The genus Hepatozoon (Apicomplexa: Adeleina). Journal of Parasitology 82, 565–585.CrossRefGoogle ScholarPubMed
Smith, TG, Desser, SS and 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 leopardo frog (Rana pipiens). Parasitology Research 80, 559–568.CrossRefGoogle Scholar
Sumrandee, C, Baimai, V, Trinachartvanit, W and Ahantarig, A (2015) Hepatozoon and Theileria species detected in ticks collected from mammals and snakes in Thailand. Ticks and Tick-Borne Diseases 6, 309–315.CrossRefGoogle ScholarPubMed
Sykes, JM IV and Klaphake, E (2008) Reptile hematology. Veterinary Clinics: Exotic Animal 11, 481–500.Google ScholarPubMed
Telford, SR Jr (2009) Hemoparasites of the Reptilia: Color Atlas and Text. Boca Raton: CRC Press.Google Scholar
Telford, SR Jr, Wozniak, EJ and Butler, JF (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.CrossRefGoogle Scholar
Trifinopoulos, J, Nguyen, LT, Von Haeseler, A and Minh, BQ (2016) W-IQ-TREE: a fast-online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44, 232–235.CrossRefGoogle ScholarPubMed
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, 670–672.CrossRefGoogle ScholarPubMed
Úngari, LP, Santos, AL, O'Dwyer, LH, Da Silva, MR, Santos, TC, Da Cunha, MJ and Cury, MC (2018) Molecular characterization and identification of Hepatozoon species Miller, 1908 (Apicomplexa: Adeleina: Hepatozoidae) in captive snakes from Brazil. Parasitology Research 117, 3857–3865.CrossRefGoogle ScholarPubMed
Úngari, LP, Netherlands, EC, De Alcantara, EP, Emmerich, E and Da Silva, RJ (2021) Description of a new species Hepatozoon quagliattus sp. nov. (Aplicomplexa: Adeleorina: Hepatozoidae), infecting the sleep snake, Dipsas mikanii (Squamata: Colubridae: Dipsadinae) from Goiás State, Brazil. Acta Parasitologica 66, 871–880.CrossRefGoogle Scholar
Viana, LA, Soares, P, Paiva, F and Lourenço-de-Oliveira, R (2010) Caiman-biting mosquitoes and the natural vectors of Hepatozoon caimani in Brazil. Journal of Medical Entomology 47, 670–676.CrossRefGoogle ScholarPubMed
Vilcins, IME, Ujvari, B, Old, JM 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 95, 434–442.CrossRefGoogle ScholarPubMed
Votýpka, J, Modrý, D, Oborník, M, Slapeta, J and Lukes, J (2017) Apicomplexa. In Archibald, JM, Simpson, GB and Slamovits, CH (eds), Handbook of the Protists. Boston: EUA, pp. 1–58.Google Scholar
Yuki, RN and Lema, T (2005) Análise comparativa entre as cobras d’água meridionais (Helicops carinicaudus (wied, 1825) e Helicops infrataeniatus Jan, 1865), com a descrição do crânio e hemipênis (Serpentes: Colubridae: Xenodontinae). Comunicações do Museu de Ciências e Tecnologia da PUCRS. Série Zoologia 18, 85–128.Google Scholar
Zechmeisterová, K, Javanbakht, H, Kvicerová, J and Siroký, P (2021) Against growing synonymy: identification pitfalls of Hepatozoon and Schellackia demonstrated on North Iranian reptiles. European Journal of Protistology 79, 125780. doi:10.1016/j.ejop.2021.125780.CrossRefGoogle ScholarPubMed
Supplementary material: Image

de Paula et al. supplementary material

de Paula et al. supplementary material

Download de Paula et al. supplementary material(Image)
Image 28.8 MB