Advertisement

Coccidia of Columbiformes: a taxonomic review of its Eimeriidae species and Eimeria columbinae n. sp. from Columbina talpacoti (Temminck, 1809) from Brazil

  • Carlos Nei Ortúzar-Ferreira
  • Mariana S. Oliveira
  • Jhon Lennon Genovez-Oliveira
  • Heider A. Franco
  • Sergio Thode-Filho
  • Sergian V. Cardozo
  • Águida A. Oliveira
  • Viviane M. Lima
  • Ildemar Ferreira
  • Bruno P. BertoEmail author
Protozoology - Original Paper
  • 22 Downloads

Abstract

Coccidia (Chromista: Miozoa: Eimeriidae) of columbiform birds (Aves: Columbiformes) have been described since the end of the nineteenth century; however, some of these descriptions were poorly detailed or inconclusive. In this sense, the current work makes a detailed taxonomic revision reconsidering and organizing 18 Eimeria spp. and two Isospora spp. previously described or reported of Columbiformes. Along with this, a new species of Eimeria is morphologically and molecularly identified by the mitochondrial cytochrome c oxidase subunit 1 (COI) gene and by the 18S small subunit ribosomal RNA (18S) gene from the ruddy ground-dove Columbina talpacoti (Temminck, 1809) in the Médio Paraíba region of the State of Rio de Janeiro, southeastern Brazil. Eimeria columbinae n. sp. has subspheroidal oocysts, 14.7 × 13.2 μm, with smooth, bi-layered wall, ~ 1.1 μm and length/width ratio of 1.1. Micropyle and oocyst residuum are present, but polar granule is absent. Sporocysts are ellipsoidal to slightly asymmetrical, 9.0 × 5.1 μm, with both Stieda and sub-Stieda bodies. Sporocyst residuum present and sporozoites with refractile body and nucleus. This is the 19th description of an eimerian from Columbiformes in the World, and the second to have a molecular identification of the COI and 18S genes.

Keywords

Taxonomy Morphology Sequencing Coccidia Oocysts Columbidae Médio Paraíba Region Rio de Janeiro Brazil 

Notes

Acknowledgments

We are thankful to the staff at the Instituto Federal de Educação, Ciência e Tecnologia do Rio de Janeiro (Campus Pinheiral), and the landowner at Santa Rita de Cássia in the Municipality of Barra Mansa, RJ, who allowed us to access and use some facilities during the expeditions.

Funding

This study was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Field-collecting permits were issued to B.P. Berto by SISBIO/ICMBio (license 42798-1) and CEUA/UFRRJ (protocol IV-6606250616).

References

  1. Abdel-Ghaffar F, Bashtar AR, Kamal AA (1986) Studies on Eimeria species infecting the Egyptian wild dove Streptopelia senegalensis aegyptiaca. 1. Exogenous stages. Bul Fac Scie 54:185–198Google Scholar
  2. Adriano EA, Thyssen PJ, Cordeiro NS (2000) Eimeria curvata n. sp. (Apicomplexa: Eimeriidae) in Columbina talpacoti and Scardafella squammata (Aves: Columbidae) from Brazil. Mem Inst Oswaldo Cruz 95:53–55PubMedCrossRefPubMedCentralGoogle Scholar
  3. Adriano EA, Thyssen PJ, Cordeiro NS (2003) A new species of Eimeria from the eared dove Zenaida auriculata (Aves: Columbidae) in Brazil. Acta Protozool 42:71–73Google Scholar
  4. Alyousif MS, Al-Shawa YR, Al-Asiri SS (2009) Eimeria livialis sp. n. (Apicomplexa: Eimeriidae) from the domestic pigeon, Columba livia domestica in Saudi Arabia. J Egypt Soc Parasitol 39:383–388PubMedPubMedCentralGoogle Scholar
  5. Ball SJ, Daszak P, Swinnerton KR, Jones CG, Snow KR (2012) A new species of Eimeria (Apicomplexa:Eimeriidae) from the endangered pink pigeon, Nesoenas mayeri (Prévost, 1843) Cheke, 2005 (Columbiformes) in Mauritius. Afr Zool 47:369–372CrossRefGoogle Scholar
  6. Bandyopadhyay PK, Bhakta JN, Shukla R (2006) A new Eimeria species (Protozoa: Apicomplexa: Sporozoea) from the blue rock pigeon Columba livia (Aves: Columbidae). Zoos Print J 21:2386–2387CrossRefGoogle Scholar
  7. Berto BP, Lopes CWG (2013) Distribution and dispersion of coccidia in wild passerines of the Americas. In: Ruiz L, Iglesias L (eds) Birds: evolution and behavior, breeding strategies, migration and spread of disease. Nova Science Publishers, New York, pp 47–66Google Scholar
  8. Berto BP, Flausino W, McIntosh D, Teixeira–Filho WL, Lopes CWG (2011) Coccidia of New World passerine birds (Aves: Passeriformes): a review of Eimeria Schneider, 1875 and Isospora Schneider, 1881 (Apicomplexa: Eimeriidae). Syst Parasitol 80:159–204PubMedCrossRefPubMedCentralGoogle Scholar
  9. Berto BP, McIntosh D, Lopes CWG (2014) Studies on coccidian oocysts (Apicomplexa: Eucoccidiorida). Rev Bras Parasitol Vet 23:1–15PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bhatia BB, Chauhan PPS, Arora GS, Agrawal RD (1972) Observations on some coccidian infections in birds and a mammal at the Dehli Zoo. Indian J Anim Sci 42:625–628Google Scholar
  11. Dolnik OV, Palinauskas V, Bensch S (2009) Individual oocysts of Isospora (Apicomplexa: Coccidia) parasites from avian feces: from photo to sequence. J Parasitol 95:169–174PubMedCrossRefPubMedCentralGoogle Scholar
  12. Duszynski D, Wilber P (1997) A guideline for the preparation of species descriptions in the Eimeridae. J Parasitol 83:333–336PubMedCrossRefPubMedCentralGoogle Scholar
  13. Duszynski D, Couch, L, Upton SJ (2000) The Coccidia of the World. Available from: <https://www.k-state.edu/parasitology/worldcoccidia>. Accessed 2 Jun 2019
  14. Golemansky V (1976) Three new coccidian species (Coccidia: Eimeriidae) found in wild birds from Bulgaria. Acta Protozool 15:399–404Google Scholar
  15. Grulet O, Landau I, Baccam D (1982) Les Isospora du Moineau domestique; multiplicite des especes. Ann Parasitol Hum Comp 57:209–235PubMedCrossRefPubMedCentralGoogle Scholar
  16. Hunt S, O’Grady J (1976) Coccidiosis in pigeons due to Eimeria labbeana. Aust Vet J 52:390PubMedCrossRefPubMedCentralGoogle Scholar
  17. ICZN (2012) International Commission on Zoological Nomenclature: Amendment of articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. Zookeys 219:1–10CrossRefGoogle Scholar
  18. IUCN (2019) The IUCN Red List of Threatened Species. Available from: <http://www.iucnredlist.org>. Accessed 12 Jun 2019
  19. Jamriška J, Modrý D (2012) A new species of Eimeria Schneider, 1875 (Apicomplexa: Eimeriidae) from the common wood pigeon Columba palumbus Linnaeus, 1758 (Aves: Columbidae). Acta Protozool 51:329–333Google Scholar
  20. Jirků M, Modrý D, Šlapeta JR, Koudela B, Lukeš J (2002) The phylogeny of Goussia and Choleoeimeria (Apicomplexa; Eimeriorina) and the evolution of excystation structures in coccidia. Protist 153:379–390PubMedCrossRefPubMedCentralGoogle Scholar
  21. Labbe A (1896) Recherches zoologiques, cytologiques et biologiques sur less coccidies. Arch Zool Exp Gen 24:517–654Google Scholar
  22. Malhotra MN, Ray HN (1961) On a few coccidium, Eimeria tropicalis n. sp. from the domestic pigeon, Columba livia intermedia. Proc 48th Indian Sci Cong 48:412Google Scholar
  23. Martinez GG, Santos ALF, Oliveira CQP, Moraes TI (2018) Estocagem de DNA a temperaturas variadas: Análise da concentração. Rev Saude Foco 10:42–50Google Scholar
  24. Matsubara R, Fukuda Y, Murakoshi F, Nomura O, Suzuki T, Tada C, Nakai Y (2017) Detection and molecular status of Isospora sp. from the domestic pigeon (Columba livia domestica). Parasitol Int 66:588–592PubMedCrossRefPubMedCentralGoogle Scholar
  25. McQuistion TE (1991) Eimeria palumbi, a new coccidian parasite (Apicomplexa: Eimeriidae) from the Galapagos dove (Zenaida galapagoensis). Trans Am Microsc Soc 110:178–181CrossRefGoogle Scholar
  26. Mitra AN, Das-Gupta M (1937) On a species of Eimeria (Coccidia–Sporozoa) from the intestine of a pigeon, Columba intermedia. Proc 24th Indian Sci Cong 24:291Google Scholar
  27. Nieschulz O (1935) Ueber Kokzidien der Haustauben. Zentralbl Bakteriol Mikrobiol Hyg 134:390–393Google Scholar
  28. Odum EP (1983) Ecologia. Guanabara Koogan, Rio de Janeiro, 434ppGoogle Scholar
  29. Ogedengbe ME, Qvarnstrom Y, da Silva AJ, Arrowood MJ, Barta JR (2015) A linear mitochondrial genome of Cyclospora cayetanensis (Eimeriidae, Eucoccidiorida, Coccidiasina, Apicomplexa) suggests the ancestral start position within mitochondrial genomes of eimeriid coccidia. Int J Parasitol 45:361–365PubMedPubMedCentralCrossRefGoogle Scholar
  30. Oliveira PSD, Ferreira MA, Silva LMD, Rodrigues MB, Cardozo SV, Berto BP (2017) Diversity and distribution of coccidia of wild birds in an Atlantic forest fragment area in southeastern Brazil. Rev Bras Parasitol Vet 26:457–464PubMedCrossRefPubMedCentralGoogle Scholar
  31. Piacentini VDQ, Aleixo A, Agne CE, Maurício GN, Pacheco JF, Bravo GA, Brito GRR, Naka LN, Olmos F, Posso S, Silveira LF, Betini GS, Carrano E, Franz I, Lees AC, Lima LM, Pioli D, Schunck F, Amaral FR, Bencke GA, Cohn-Haft M, Figueiredo LFA, Straube FC, Cesari E (2015) Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. Rev Brasil Ornitol 23:91–298Google Scholar
  32. Pinto C (1928) Synonymie de quelques especes du genre Eimeria (Eimeridia, Sporozoa). C R Seances Soc Biol 98:564–1565Google Scholar
  33. Ray DK (1952) On a new coccidium, Eimeria sphenocercae n. sp. , from Sphenocercus sphenurus (Kokla Green pigeon). J Parasitol 38:546–547PubMedCrossRefPubMedCentralGoogle Scholar
  34. Rodrigues MB, Oliveira JLG, Silva-Carvalho LM, Pastura DGN, Gomes JV, Oliveira MS, Siqueira PB, Oliveira AA, Lima VM, Ferreira I, Berto BP (2019) The vulnerable Sporophila frontalis (Verreaux) and Haplospiza unicolor Cabanis as new hosts for Isospora sporophilae Carvalho–Filho, Meireles, Ribeiro and Lopes, 2005 (Eimeriidae) in Brazil. Syst Parasitol 96:423–431PubMedCrossRefPubMedCentralGoogle Scholar
  35. Ruggiero MA, Gordon DP, Orrell TM, Bailly N, Bourgoin T, Brusca RC, Cavalier-Smith T, Guiry MD, Kirk PM (2015) Correction: a higher level classification of all living organisms. PLoS One 10:e0130114PubMedPubMedCentralCrossRefGoogle Scholar
  36. Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro, p 862Google Scholar
  37. Sigrist T (2014) Guia de Campo: Avifauna Brasileira. São Paulo, Avis Brasilis, 608 ppGoogle Scholar
  38. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefPubMedCentralGoogle Scholar
  39. Tenter AM, Barta JR, Beveridge I, Duszynski DW, Mehlhorn H, Morrison DA, Thompson RCA, Conrad PA (2002) The conceptual basis for a new classification of the coccidia. Int J Parasitol 32:595–616PubMedCrossRefPubMedCentralGoogle Scholar
  40. Trefancová A, Mácová A, Kvičerová J (2019) Isosporan oocysts in the faeces of bank voles (Myodes glareolus; Arvicolinae, Rodentia): real parasites, or pseudoparasites? Protist 170:104–120PubMedCrossRefPubMedCentralGoogle Scholar
  41. Varghese T (1978a) Isospora gallicolumbae sp. n. from Beccari’s ground dove (Gallicolumba beccarii Salvadori) in Papua New Guinea. J Protozool 25:425–426PubMedCrossRefPubMedCentralGoogle Scholar
  42. Varghese T (1978b) Eimeria waiganiensis sp. n. from the Greenwinged Ground dove (Chalcophaps indica Linnaeus) and the magnificent Ground pigeon (Otidiphaps nobilis Gould) in Papua New Guinea. J Parasitol 64:312–314PubMedCrossRefPubMedCentralGoogle Scholar
  43. Varghese T (1980) Coccidian parasites of birds of the avian order Columbiformes with a description of two new species of Eimeria. Parasitol 80:183–187CrossRefGoogle Scholar
  44. Williams RB, Thebo P, Marshall RN, Marshall JA (2010) Coccidian oöcysts as type–specimens: long–term storage in aqueous potassium dichromate solution preserves DNA. Syst Parasitol 76:69–76PubMedCrossRefPubMedCentralGoogle Scholar
  45. Xavier R, Santos JL, Verissimo A (2018) Phylogenetic evidence for an ancestral coevolution between a major clade of coccidian parasites and elasmobranch hosts. Syst Parasitol 95:367–371PubMedCrossRefPubMedCentralGoogle Scholar
  46. Yabsley MJ, Bailey K, Adams HC (2015) A New Species of Eimeria (Apicomplexa: Eimeriidae) from the Mourning Dove, Zenaida macroura (Columbiformes: Columbidae). Comp Parasitol 82:231–234CrossRefGoogle Scholar
  47. Yang R, Brice B, Elliot A, Ryan U (2015) Isospora serinuse n. sp. (Apicomplexa: Eimeriidae) from a domestic canary (Serinus canaria forma domestica) (Passeriformes: Fringillidae) in Western Australia. Exp Parasitol 159:59–66PubMedCrossRefPubMedCentralGoogle Scholar
  48. Yang R, Brice B, Elloit A, Ryan U (2016) Morphological and molecular characterization of Eimeria labbeana–like (Apicomplexa:Eimeriidae) in a domestic pigeon (Columba livia domestica, Gmelin, 1789) in Australia. Exp Parasitol 166:124–130PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Carlos Nei Ortúzar-Ferreira
    • 1
  • Mariana S. Oliveira
    • 2
  • Jhon Lennon Genovez-Oliveira
    • 2
  • Heider A. Franco
    • 3
  • Sergio Thode-Filho
    • 3
    • 4
  • Sergian V. Cardozo
    • 5
  • Águida A. Oliveira
    • 6
  • Viviane M. Lima
    • 6
  • Ildemar Ferreira
    • 6
  • Bruno P. Berto
    • 6
    Email author
  1. 1.Curso de Graduação em Medicina Veterinária, Instituto de VeterináriaUniversidade Federal Rural do Rio de Janeiro (UFRRJ)SeropédicaBrazil
  2. 2.Programa de Pós-Graduação em Biologia AnimalInstituto de Ciências Biológicas e da Saúde (ICBS), UFRRJSeropédicaBrazil
  3. 3.Instituto Federal de Educação, Ciência e Tecnologia do Rio de JaneiroPinheiralBrazil
  4. 4.Programa de Pós-graduação em Ciência, Tecnologia e Inovação em AgropecuáriaUFRRJSeropédicaBrazil
  5. 5.Programa de Pós-Graduação em Biomedicina TranslacionalUniversidade do Grande RioDuque de CaxiasBrazil
  6. 6.Departamento de Biologia AnimalICBS, UFRRJSeropédicaBrazil

Personalised recommendations