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Parasitology Research

, Volume 117, Issue 5, pp 1535–1548 | Cite as

Haemogregarina podocnemis sp. nov.: description of a new species of Haemogregarina Danilewsky 1885 (Adeleina: Haemogregarinaidae) in free-living and captive yellow-spotted river turtles Podocnemis unifilis (Testudines: Podocnemididae) from Brazil

  • Letícia Pereira Úngari
  • André Luiz Quagliatto Santos
  • Lucia Helena O’Dwyer
  • Maria Regina Lucas da Silva
  • Natália Nasser de Melo Fava
  • Guilherme Carrara Moreira Paiva
  • Rogério de Melo Costa Pinto
  • Márcia Cristina Cury
Original Paper

Abstract

Based on morphological, morphometric, and molecular data, we describe a new hemoparasite of the genus Haemogregarina Danilewsky 1885, isolated from the Brazilian aquatic turtle Podocnemis unifilis (Testudines: Podocnemididae). The new species, Haemogregarina podocnemis sp. nov. (Apicomplexa: Haemogregarinidae), is characterized by small trophozoites with a single cytoplasmic vacuole on one side; pre-meronts with nuclear chromatin dispersed in the cytoplasm, with or without cytoplasmic vacuoles; meronts that are usually broad and slightly curved (kidney-shaped), with an average of eight small rectangular nuclei; immature gamonts (bean-shaped) with two morphological types: one with nuclear chromatin dispersed in the cytoplasm and the other with nuclei in the middle of the cell; mature gamonts of two morphological types: one with a length equal to or greater than that of the erythrocyte and the width of the nuclei similar to that of the hemoparasite and the other smaller than the erythrocyte with the width of the nuclei less than that of the hemoparasite. This is the first hemogregarine species described that infects the Brazilian turtle Po. unifilis. These findings highlight the need for further studies of Haemogregarina spp. to better determine the biodiversity of this understudied parasite group.

Keywords

Haemogregarina Podocnemis unifilis Turtle 

Notes

Acknowledgments

We thank the team at the Laboratory for Teaching and Research in Wild Animals (LAPAS) and the veterinarians at Exotic Life, Rodrigo Rabello and Matheus Rabello, for their assistance in the collection of blood from turtles. We thank Prof. Dr. Lúcio André Viana Dias and Amanda Picelli for providing a positive control for the molecular assay.

Funding information

We thank Coordination for the Improvement of Higher Education Personnel (CAPES) and Research Foundation of the State of Minas Gerais (FAPEMIG) for their financial support.

Compliance with ethical standards

The project was submitted to and approved by the Ethics Committee for Animal Use (CEUA) at the Federal University of Uberlândia, Uberlândia, Minas Gerais, Brazil, (protocol 032/16) and by the Biodiversity Information and Authorization System (SISBIO) (Protocol 51398-1).

References

  1. Alhaboubi AR, Pollard DA Holman PJ (2017) Molecular and morphological characterization of a haemogregarine in the alligator snapping turtle, Macrochelys temminckii (Testudines: Chelydridae). Parasitol Res 116:207–215CrossRefPubMedGoogle Scholar
  2. Amo L, López P, Martin J (2005) Prevalence and intensity of haemogregarine blood parasites and their mite vectors in the common wall lizard, Podarcis muralis. Parasitol Res 96:378–381CrossRefPubMedGoogle Scholar
  3. Araújo JC, Palha MDC, Rosa PV (2013) Nutrição na Quelonicultura—Revisão. Rev Elet Nutrit 10:2828–2871Google Scholar
  4. Arizza V, Sacco F, Russo D, Scardino R, Arculeo M, Vamberger M, Marrone F (2016) The good, the bad and the ugly: Emys trinacris, Placobdella costata and Haemogregarina stepanowi in Sicily (Testudines, Annelida and Apicomplexa. Folia Parasitol 63Google Scholar
  5. Barta JR, Ogedengbe JD, Martin DS, Smith TG (2012) Phylogenetic Position of the Adeleorinid Coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) Inferred Using 18S rDNA Sequences. J Eukaryot Microbiol 59:171–180CrossRefPubMedGoogle Scholar
  6. Bérnils RS, Costa HC (2012) Brazilian reptiles: list of species. Soc. Bras. de Herpet. http://www.sbherpetologia.org.br. Accessed 13 March 2014
  7. Biase NG, Ferreira DF (2009) Comparações múltiplas e testes simultâneos para parâmetros binomiais de K populações independentes. Ver Bras Biom 27:301–323Google Scholar
  8. Borges-Nojosa DM, Borges-Leite MJ, Maia JP, Zanchi-Silva D, da Rocha Braga R, Harris DJ (2017)A new species of Hepatozoon Miller, 1908 (Apicomplexa: Adelerina) from the snake Philodryas nattereri Steindachner (Squamata: Dipsadidae) in northeastern Brazil Syst Parasitol 94: 65–72Google Scholar
  9. Brown MJF, Loosli R, Hampel SP (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91:421–427CrossRefGoogle Scholar
  10. Campos-Brites VL, Rantin FT (2004) The influence of agricultural and urban contamination on leech infestation of freshwater turtles, Phrynops geoffroanus, taken from two areas of the Uberabinha river. Environ Monit Asses 96:273–281CrossRefGoogle Scholar
  11. Cook CA, Lawton SP, Davies AJ, Smit NJ (2014) Ressignment of the land tortoise haemogregarine Haemogregarina fitzsimonsi Dias 1953 (Adeleorina: Haemogregarinidae) to the genus Hepatoozon Miller 1908 (Adeleorina: Hepatozoidae) based on parasite morphology, life cycle and phylogenetic analysis of 18S r DNA sequences fragments. Parasitology 141:1611–1620CrossRefGoogle Scholar
  12. Cook CA, Netherlands EC, Smit NJ (2015) First Hemolivia from southern Africa: reassigning chelonian Haemogregarina parvula Dias, 1953 (Adeleorina: Haemogregarinidae) to Hemolivia (Adeleorina: Karyolysidae). Afr Zool 50:165–173CrossRefGoogle Scholar
  13. Coutinho ME (2003) Population ecology and the conservation and management of Caiman yacare in the Pantanal, Brazil. Dissertation, Universidade de QueenslandGoogle Scholar
  14. Crawford RLDVM (2008) Information resources on reptiles. National Agricultural Library, MarylandGoogle Scholar
  15. Criado-Fornelio A, Martinez-Marcos A, Buling-Sarana A, Barba-Carretero JC (2003) Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe. Part I. Epizootiological aspects. Vet Parasitol 113:189–201CrossRefPubMedGoogle Scholar
  16. Criado-Fornelio A, Ruas JL, Casado N, Farias NA, Soares MP, Muller G, Brumt JG, Berne ME, Buling-Sarana A, Barba-Carretero JC (2006) New molecular data on mammalian Hepatozoon species (Apicomplexa: Adeleorina) from Brazil and Spain. Int J Parasitol 92:93–99CrossRefGoogle Scholar
  17. Dariba D, Toboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefGoogle Scholar
  18. Davies AK, Johnston MRL (2000) The biology of some intraerithrocytic parasites of fishes, amphibian and reptiles. Adv Parasitol 45:1–107CrossRefPubMedGoogle Scholar
  19. Davies AK, Sterrett S (2011) Prevalence of haemogregarine parasites in three freshwater turtles species in a population in northeast Georgia, USA. Int J Zoo Res 7:156–163CrossRefGoogle Scholar
  20. Davies AJ, Smith NJ, Hayes PM, Seddon AM, Wertheim D (2004) Haemogregarina bigemina (Protozoa: Apicomplexa: Adeleorina) past, present and future. Folia Parasitol 51:99–108CrossRefPubMedGoogle Scholar
  21. Demoner LC, Magro NM, Da Silva MR, De Paula Antunes JM, Calabuig CI, O'Dwyer LH (2016) Hepatozoon spp. infections in wild rodents in an area of endemic canine hepatozoonosis in southeastern Brazil Ticks. Tick Borne Dis 7:859–864CrossRefGoogle Scholar
  22. Dvoráková N, Kvicerová J, Papoušek I, Javanbakht H, Tiar G, Kami H, Široký P (2014) Haemogregarines from western Palaearctic freshwater turtles (genera Emys, Mauremys) are conspecific with Haemogregarina stepanowi Danilewsky, 1885. Parasitology. 141(4):522–30CrossRefPubMedGoogle Scholar
  23. Dvoráková N, Kvicerová J, Hostovský M, Siroký P (2015) Haemogregarines of freshwater turtles from Southeast Asia with a description of Haemogregarina sacaliae sp. n. and a redescription of Haemogregarina pellegrini Laveran and Pettit, 1910. J Parasitol 142:816–826CrossRefGoogle Scholar
  24. Eisen RJ, Schall JJ (2000) Life history of malaria parasite (Plasmodium mexicanum): independent traits and basis for variation. Proc Biol Sci 267:793–799CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ferrari AS (1980) Quelônios: animais em extinção. Manaus, FalangolaGoogle Scholar
  26. Garcia-Navarro CEK, Pachalli JR (1994) Manual de hematologia veterinária. Livraria Varela, São PauloGoogle Scholar
  27. Godfrey RD Jr, Fedynich AM, Pence DB (1987) Quantification of haemotozoa in blood smears. J Wildlife Dis 23:558–565CrossRefGoogle Scholar
  28. 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 59:307–321CrossRefPubMedGoogle Scholar
  29. 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. Parasitology 141:389–398CrossRefGoogle Scholar
  30. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Ac Symp Series 41:95–98Google Scholar
  31. Ibama – Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (1989) Projeto Quelônios da Amazônia—10 anos. IBAMA, BrasíliaGoogle Scholar
  32. Jakes KA, O’Donoghue P, Munro M, Adlard R (2001) Hemoprotozoa of fresh turtles in Queensland. J Wildl Dis 37:12–19CrossRefPubMedGoogle Scholar
  33. Kopecna J, Jirku M, Obornik M, Tokarev YS, Lukes J, Modry D (2006) Phylogenetic analysis of coccidian parasites from invertebrates: search for missing links. Protist 157:173–183CrossRefPubMedGoogle Scholar
  34. Kvičerová J, Pakandl M, Hypša V (2008) Phylogenetic relationships among Eimeria spp. (Apicomplexa, Eimeriidae) infecting rabbits: evolutionary significance of biological and morphological features. Parasitol 135:443–452Google Scholar
  35. Kvicerova J, Hypsa V, Dvorakova N, Mikulicek P, Jandzik D, Gardner MG, Javanbakht H, Tiar G (2014) Siroky P. H emolivia and Hepatozoon: Haemogregarines with Tangled Evolutionary Relationships Protist 165:688–700Google Scholar
  36. Lainson R, Naiff R (1998) Haemoproteus (Apicomplexa: Haemoproteidae) of tortoises and turtles. Proc R Soc B 265:941–949CrossRefPubMedPubMedCentralGoogle Scholar
  37. Levine ND (1988) The protozoan phylum Apicomplexa. CRC Press, Boca RatonGoogle Scholar
  38. Maia JP, Harris DJ, Perera A (2011) Molecular survey of Hepatozoon Species in Lizards From North Africa. J Parasitol 97:513–517CrossRefPubMedGoogle Scholar
  39. Maia JP, Pereira A, Harris DJ (2012) Molecular survey and microscopic examination of Hepatozoon Miller, 1908 (Apicomplexa: Adeleorina) in lacertid lizards from western Meditarranean. Folia Parasitol 59:241–248CrossRefPubMedGoogle Scholar
  40. Maia JP, Harris DJ, Carranza S, Gómez-Días E (2014) A comparison of methods for estimating parasitemia of hemoparasites (Apicomplexa: Adeleorina) and its application for studying infection in natural populations. PLoS One 9:1–10Google Scholar
  41. Maia JP, Harris DJ, Carranza S, Goméz-Días E (2016) Assessing the diversity, host-specificity and infection patterns of apicomplexan parasites in reptiles from Oman, Arabia. Parasitology 143:1730–1747CrossRefPubMedGoogle Scholar
  42. Malvasio A, Souza AM, Gomes N, Sampaio FAA, Molina FB (2002) Variações ontogenéticas na morfometria e morfologia do canal alimentar pós-faríngeo de Trachemys dorbignyi (Duméril e Bibron, 1835) Podocnemis expansa (Schweigger, 1812), P. unifilis (Troschel, 1848) P. sexturberculata (Cornalia, 1849) (Anapsida: Testudines). PblAvul Inst Pau Bras His Nat 5:39–51Google Scholar
  43. Mathew JS, Van Den Bussche RA, Ewing SA, Malayer JR, Latha BR, Panciera RJ (2000) Phylogenetic relationships of Hepatozoon (Apicomplexa: Adeleorina) based on molecular, morphologic, and lifecycle characters. J Parasitol 86:366–372CrossRefPubMedGoogle Scholar
  44. McAllister CT, Bursey CR, Robison HW, Connior MB, Barger MA (2014) Haemogregarina sp. (Apicomplexa: Haemogregarinidae) Telorchis attenuate (Digenea: Telorchiidae) and Neoechinorhynchus mauydis (Acanthocephala: Neoechinorhynchidae) form map turtles (Graptemys spp.), in northcentral Arkansas. J Ark Acad Sci 68:154–157Google Scholar
  45. McCoy JC, Failey E, Price SJ, Dorcas ME (2007) An assessment of leech parasitism on semi-aquatic turtles in the Eastern Piedmont of North Carolina. Southeast Nat 6:191–202CrossRefGoogle Scholar
  46. Mihalca AD, Achelaripei D, Popescu P (2002) Haemoparasites to the genus Haemogregarina in a population of European pond turtles (Emys orbicularis) from Dragasani, Valcea country, Romenia. Rev Sci Parasitol 3:22–27Google Scholar
  47. Moço TC, O’Dwyer LH, Vilela FC, Barella TH, Silva RJ (2002) Morphologic and morphometric analysis of Hepatozoon spp. (Apicomplexa, Hepatozoidae) of snakes. Mem Inst Oswaldo Cruz 97:1169–1176CrossRefPubMedGoogle Scholar
  48. Moço TC, Silva RJ, Madeira NG, Dos Santos PK, Rubini AS, Leal DD, O’Dwyer LH (2012) Prevalência de Hepatozoon spp. em serpentes e caracterização morfológica, morfométrica e molecular de Hepatozoon (Apicomplexa, Hepatozoidae) de Crotalus durissus terrificus (Serpentes, Viperidae) naturalmente infectadas. Parasitol Res 110:1393–1401CrossRefPubMedGoogle Scholar
  49. Møller AP (1997) Parasitism and the evolution of host life history. In: Clayton DH, Moore J (eds) Host–parasite evolution: general principals and avian models. Oxford University Press, Oxford, pp 105–127Google Scholar
  50. O’Dwyer LH, Moço TC, Paduan S, Spenassatto C, Silva RJ, Ribolla PE (2013) Description of three new species of Hepatozoon (Apicomplexa, Hepatozoidae) from rattlesnakes (Crotalus durissus terrificus) based on molecular, morphometric and morphologic characters. Exp Parasitol 135:200–207CrossRefPubMedGoogle Scholar
  51. Olsson M, Wapstra E, Madsen T, Ujvari B, Rugfelt C (2005) Costly parasite resistance: a genotype-dependent handicap in sand lizards? Biol Lett 1:375–377CrossRefPubMedPubMedCentralGoogle Scholar
  52. Oppliger A, Clobert J (1997) Reduced tail regeneration in the common lizard, Lacerta vivipara, parasite by blood parasites. Fund Ecol 11:652–655CrossRefGoogle Scholar
  53. Oppliger A, Célérier ML, Clobert J (1996) Physiological and behavioral changes in common lizards parasite by haemogregarines. Parasitology 133:433–438CrossRefGoogle Scholar
  54. 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. Clin Diagn Lab Immunol 12:1343–1346PubMedPubMedCentralGoogle Scholar
  55. Ozvegy J, Marinkovic D, Vucicevic M, Gajic B, Stevanovic J, Marinkovic D, Stevanovic J, Krnjaic D, Aleksic Kovacevic S (2015) Cytological and molecular identification of Haemogregarina stepanowi in blood samples of the European pond turtle (Emys orbicularis) from quarantine at Belgrade zoo. Acta Vet 65:443–453CrossRefGoogle Scholar
  56. Perkins SL, Keller AK (2001) Phylogeny of nuclear small subunit rRNA genes of haemogregarines amplified with specific primers. J Parasitol 87:870–876CrossRefPubMedGoogle Scholar
  57. Pessoa LMB, Scalon MC, Carneiro FT, Lima MGM, Silva TF, Monteiro RV, Paludo GR (2016) Ocorrência de hemogregarina em duas espécies de cágados brasileiros. Acta Sci Vet 44:1381Google Scholar
  58. Picelli AM, Carvalho AV, Viana LA, Malvasio A (2015) Prevalence and parasitemia of Haemogregarina sp. in Podocnemis expansa (Testudines: Podocnemididae) from the Brazilian Amazon. Parasitol Res 113:4499–4503Google Scholar
  59. Portelinha TCG, Malvasio A, Piña CI, Bertoluci JA (2013) Reproductive allometry of Podocnemis expansa (Testudines: Podocnemididae) in southern Brazilian Amazon. J Herpetol 47:232–236CrossRefGoogle Scholar
  60. Readel AM, Philliphs CA, Wetzel MJ (2008) Leech parasitism in a turtle assemblage: effects of hot and environmental characteristics. Copeia 2008(1):227–233CrossRefGoogle Scholar
  61. Salera-Junior G, Malvasio A (2005) Biologia e Conservação dos Quelônios da Amazônia. Universidade Federal do Tocantins, PalmasGoogle Scholar
  62. Sandland GJ, Minchella DJ (2003) Costs of immune defense: an enigma wrapped in an environmental cloack? Trend Parasitol 19:571–574CrossRefGoogle Scholar
  63. Sehgal RN, Jones HI, Smith TB (2005) Blood parasites of some west African rainforest birds. J Vet Med Sci 67:295–301CrossRefPubMedGoogle Scholar
  64. Siddal ME, Desser SS (1993) Ultrastructure of merogonic development of Haemogregarina (sensulato) myoxocephali (Apicomplexa: Adeleorina) in the marine leech Malmiana scorpii and localization of infective stages in the salivary cells. Eur J Protistol 29:191–201CrossRefGoogle Scholar
  65. Siddall ME (1995) Phylogeny of Adeleid blood parasites with a partial systematic revision of the haemogregarine complex. J Eukaryot Microbiol 24:1161–1125Google Scholar
  66. Siddall ME, Desser SS (1991) Merogonic development of Haemogregarina balli (Apicomplexa: Adeleorina: Haemogregarinidae) in the leech Placobdella ornate (Glossiphoniidae), its transmission to a chelonian intermediate host and phylogenetic implications. J Parasitol 77:426–436CrossRefGoogle Scholar
  67. Siddall ME, Desser SS (1992) Prevalence and intensity of Haemogregarinaballi (Apicomplexa: Adeleorina: Haemogregarinidae) in three turtles species from Ontario, with observations on intraerythrocytic development. Can J Zool 70:123–128CrossRefGoogle Scholar
  68. Siddall ME, Desser SS (2001) Transmission of Haemogregarina balli from painted turtles to snapping turtles through the leech Plocobdella ornate. J Parasitol 87:1217–1218CrossRefPubMedGoogle Scholar
  69. Siroký P, Kamler M, Modrý D (2004) Long-term occurrence of Hemolivia cf. mauritanica (Apicomplexa: Adeleina: Haemogregarinidae) in captive Testudo marginata (Reptilia: Tetsudinidae): evidence for cyclic merogony? J Parasitol 90:1391–1393CrossRefPubMedGoogle Scholar
  70. 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. J Parasitol 93:1189–1198CrossRefPubMedGoogle Scholar
  71. Soares P, Brito ES, Paiva F, Pavan D, Viana LA (2014) Haemogregarina spp. in wild population from Podocnemis unifilis Trschel, 1848 in the Brazilian Amazon. Braz J Vet Parasitol 24:191–197Google Scholar
  72. Telford SR Jr (1971) Parasitic diseases of reptiles. J Am Vet Med Assoc 159:1644–1652PubMedGoogle Scholar
  73. Telford SR Jr (2009) Hemoparasites of the reptilian: color atlas and text. CRC Press, Boca RatonGoogle Scholar
  74. Thrall PH, Hochberg ME, Burdon JJ, Bever JD (2007) Coevolution of symbiotic mutualists and parasites in a community context. Trend Eco Evol 22:120–126CrossRefGoogle Scholar
  75. Ujvari B, Marques EJ (2005) High prevalence of Hepatozoon spp. (Apicomplexa: Hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia. J Parasitol 90:670–672CrossRefGoogle Scholar
  76. Vogt RC (2008) Tartarugas da Amazônia. Biblos, LimaGoogle Scholar
  77. Wosniak EJ, Mclaughlin GL, Telford SR (1994) Description of the vertebrate stages of a hemogregarine species naturally infecting Mojave Desert sidewinders (Crotalus cerastes cerastes). J Zoo Wildl Med 25:103–110Google Scholar
  78. Zippel KC, Lillywhite HB, Mladinich CRJ (2001) New vascular system in reptiles: anatomy and postural hemodynamics of the vertebral venous plexus in snakes. J Morphol 250:173–184CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Letícia Pereira Úngari
    • 1
    • 2
  • André Luiz Quagliatto Santos
    • 3
  • Lucia Helena O’Dwyer
    • 2
  • Maria Regina Lucas da Silva
    • 2
  • Natália Nasser de Melo Fava
    • 1
  • Guilherme Carrara Moreira Paiva
    • 3
  • Rogério de Melo Costa Pinto
    • 4
  • Márcia Cristina Cury
    • 1
  1. 1.Laboratório de Parasitologia, Instituto de Ciências BiomédicasUniversidade Federal de UberlândiaUberlândiaBrazil
  2. 2.Instituto de Biociências, Campus de Botucatu, Departamento de ParasitologiaUNESP-Univ Estadual PaulistaBotucatuBrazil
  3. 3.Laboratório de Ensino e Pesquisa em Animais Silvestres, Faculdade de Medicina VeterináriaUniversidade Federal de UberlândiaMinas GeraisBrazil
  4. 4.Faculdade de Matemática-FAMAT, Centro de Ciências e TecnologiaUniversidade Federal de Uberlândia—UFUUberlândiaBrazil

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