Advertisement

Parasitology Research

, Volume 118, Issue 10, pp 2819–2829 | Cite as

An integrative taxonomic assessment of Procamallanus (Spirocamallanus) huacraensis (Nematoda: Camallanidae), infecting the freshwater catfish Trichomycterus spegazzinii (Siluriformes: Trichomycteridae) in Argentina

  • Lorena G. Ailán-Choke
  • Dora A. Davies
  • Luiz E.R. Tavares
  • Felipe B. PereiraEmail author
Fish Parasitology - Original Paper
  • 99 Downloads

Abstract

Procamallanus (Spirocamallanus) huacraensis infecting the catfish Trichomycterus spegazzinii from Escoipe River, Salta province (Argentina), is redescribed and genetically characterised for the first time, based on three genetic markers (nuclear 18S and 28S rRNA; cytochrome c oxidase subunit I [cox1] mtDNA). The phylogeny of Camallanidae was also discussed. Morphological evaluation of P. (S.) huacraensis using light and scanning electron microscopy revealed the previously undescribed features: location of deirids, accurate morphology of larvae (L1) and ovijector in females, as well as phasmids in males. Differences were found comparing the newly collected material and the type specimens, probably because the original description lacked detailing. Unfortunately, type specimens of P. (S.) huacraensis were no available for loan. The results of morphological and genetic analyses supported the validity of P. (S.) huacraensis. Inconsistencies regarding the taxonomic identification of species of Camallanidae in GenBank database were noted. Based on the current genetic database of Camallanidae, phylogenetic reconstructions using the 18S rRNA sequences were most consistent, due to the inclusion of higher number of taxa. Procamallanus (S.) huacraensis appeared as sister group of P. (S.) rarus, also isolated from a catfish in a neighbouring region. The order and habitat of hosts were also similar within some well-supported parasite lineages, but without common geographic origin. However, it is still premature to make definitive affirmations regarding the role of such features in the phylogenetic patterns of Camallanidae, given the scarcity of genetic data. The phylogenetic reconstructions also confirmed the artificiality of the morphology-based systematics of the family.

Keywords

Nematode parasite Genetic characterisation Phylogeny Neotropical region 

Notes

Acknowledgements

The authors would like to thank Dr. Elias Nogueira de Aguiar from the Laboratório Multiusuário de Análises de Materiais do Instituto de Física (MULTILAM-INFI), from the Universidade Federal de Mato Grosso do Sul (UFMS), for the help with scanning electron microscopical procedures, and Dr. Carina Elisei from the Universidade Católica Dom Bosco, for providing the facilities for molecular studies. Thanks are also due to the Secretaría de Medio Ambiente del Gobierno de la Provincia de Salta for allowing us to make the collection of ichthyology, and Florencia Liquín, José Saravia, Roberto Sanchez, Federico Soria and Facundo Leguizamon for their assistance in the field work.

Funding information

This work was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance code 001 and by the Consejo de Investigación de la Universidad Nacional de Salta (CIUNSa) (grant number 2193/3). F. B. P. was supported by a Post-doctoral fellowship PNPD-CAPES (Programa Nacional de Pós-Doutorado-Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES, Brazil). L. A. C. was supported by a Doctoral fellowship from the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina); L. E. R. T. was supported by a researcher’s fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) (313292/2018-3).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

436_2019_6429_MOESM1_ESM.pdf (288 kb)
ESM 1 (PDF 288 kb)
436_2019_6429_MOESM2_ESM.pdf (28 kb)
ESM 2 (PDF 28 kb)
436_2019_6429_MOESM3_ESM.pdf (127 kb)
ESM 3 (PDF 126 kb)
436_2019_6429_MOESM4_ESM.pdf (49 kb)
ESM 4 (PDF 48 kb)

References

  1. Anderson RC, Chabaud AG, Willmott S (2009) Keys to the nematode parasites of vertebrates: archival volume. CABI Publishing, WallingfordCrossRefGoogle Scholar
  2. Černotíková E, Horák A, Moravec F (2011) Phylogenetic relationships of some spirurine nematodes (Nematoda: Chromadorea: Rhabditida: Spirurina) parasitic in fishes inferred from SSU rRNA gene sequences. Folia Parasitol 58:135–148.  https://doi.org/10.14411/fp.2011.013 CrossRefPubMedGoogle Scholar
  3. Chang J-M, Di Tommaso P, Notredame C (2014) TCS: a new multiple sequence alignment reliability measure to estimate alignment accuracy and improve phylogenetic tree reconstruction. Mol Biol Evol 31:1625–1637.  https://doi.org/10.1093/molbev/msu117 CrossRefPubMedGoogle Scholar
  4. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772.  https://doi.org/10.1038/nmeth CrossRefPubMedPubMedCentralGoogle Scholar
  5. Freitas JFT, Ibáñez HN (1968) Fauna helmintológica del Perú: nueva especie del género Spirocamallanus Olsen, 1952 (Nematoda, Camallanoidea). Bol Chil Parasitol 23:146–148Google Scholar
  6. Froese R, Pauly D (Eds) (2019) FishBase. World Wide Web electronic publication. http://www.fishbase.org, version 02/2019. Accessed 22 Feb 2019
  7. Gaither MR, Aeby G, Vignon M, Meguro Y, Rigby M, Runyon C, Toonen RJ, Wood CL, Bowen BW (2013) An invasive fish and the time-lagged spread of its parasite across the Hawaiian archipelago. PLoS One 8:e56940.  https://doi.org/10.1371/journal.pone.0056940 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Giese EG, Santos JN, Lanfredi RM (2009) A new species of Camallanidae from Ageneiosus ucayalensis (Pisces: Siluriformes) from Pará state, Brazil. J Parasitol 95:407–412.  https://doi.org/10.1645/GE-1680.1 CrossRefPubMedGoogle Scholar
  9. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704.  https://doi.org/10.1080/10635150390235520 CrossRefPubMedGoogle Scholar
  10. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755.  https://doi.org/10.1093/bioinformatics/17.8.754 CrossRefPubMedGoogle Scholar
  11. Kuzmin Y, Tkach VV, Snyder SD, Bell JA (2011) Camallanus Railliet et Henry, 1915 (Nematoda, Camallanidae) from Australian freshwater turtles with descriptions of two new species and molecular differentiation of known. Acta Parasitol 56:213–226.  https://doi.org/10.2478/s11686-011-0015-0 CrossRefGoogle Scholar
  12. Moravec F (1998) Nematodes of freshwater fishes of the Neotropical region. Academia, PrahaGoogle Scholar
  13. Moravec F, Chara J, Shinn AP (2004) Two nematodes, Dentinema trichomycteri n. g., n. sp. (Cosmocercidae) and Procamallanus chimusensis Freitas & Ibáñez, 1968 (Camallanidae), from catfishes Trichomycterus spp. (Pisces) in Colombia. Syst Parasitol 59:189–197.  https://doi.org/10.1023/B:SYPA.0000048098.80098.26 CrossRefPubMedGoogle Scholar
  14. Moravec F, Justine J-L, Würtz J, Taraschewski H, Sasal P (2006) A new species of Procamallanus (Nematoda: Camallanidae) from Pacific eels (Anguilla spp.). J Parasitol 92:130–137.  https://doi.org/10.1645/GE-3509.1 CrossRefPubMedGoogle Scholar
  15. Moravec F, Justine J-L (2017) Two new species of nematode parasites, Cucullanus epinepheli sp. n. (Cucullanidae) and Procamallanus (Spirocamallanus) sinespinis sp. n. (Camallanidae), from marine serranid and haemulid fishes off New Caledonia. Folia Parasitol 64(011).  https://doi.org/10.14411/fp.2017.011
  16. Moravec F, Sey O (1988) Nematodes of freshwater fishes from North Vietnam. Part 1. Camallanoidea and Habronematoidea. Acta Soc Zool Bohemoslov 52:128–148Google Scholar
  17. Moravec F, Thatcher VE (1997) Procamallanus (Denticamallanus subgen. n.) dentatus n. sp. (Nematoda: Camallanidae) from the characid fish, Bryconops alburnoides, in the Brazilian Amazon. Parasite 4:239–243CrossRefGoogle Scholar
  18. Moravec F, Van As LL (2015) Procamallanus (Spirocamallanus) spp. (Nematoda: Camallanidae) from fishes of the Okavango River, Botswana, including P. (S.) serranochromis n. sp. parasitic in Serranochromis spp. (Cichlidae). Syst Parasitol 90:151–164.  https://doi.org/10.1007/s11230-014-9542-z
  19. Notredame C, Higgins DG, Heringa J (2000) T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217.  https://doi.org/10.1006/jmbi.2000.4042 CrossRefPubMedGoogle Scholar
  20. Ramallo G (2008) Nueva especie de Procamallanus (Spirocamallanus) (Nematoda, Camallanidae), parásito de Trichomycterus corduvensis (Siluriformes: Trichomycteridae), en el Norte de Argentina. Acta Zool Lilloana 52:25–29Google Scholar
  21. Ramallo G, Padilla Bortayro G (2011) Nemátodos parásitos de peces dulceacuícolas de la Provincia de Catamarca, Argentina. Acta Zool Lilloana 55:261–263Google Scholar
  22. Rigby MC, Adamson ML (1997) Spirocamallanus species of French Polynesian coral reef fishes. Can J Zool 75:1270–1279.  https://doi.org/10.1139/z97-150
  23. Sardella CJ, Pereira FB, Luque JL (2017) Redescription and first genetic characterisation of Procamallanus (Spirocamallanus) macaensis Vicente & Santos, 1972 (Nematoda: Camallanidae), including re-evaluation of the species of Procamallanus (Spirocamallanus) from marine fishes off Brazil. Syst Parasitol 94:657–668.  https://doi.org/10.1007/s11230-017-9728-2 CrossRefPubMedGoogle Scholar
  24. Tantaleán VM, Franco AH, Huayta EH (1985) Helmintos parásitos de peces de agua dulce del Perú. Instituto de Investigaciones para el Desarrollo Social del Altiplano, PunoGoogle Scholar
  25. Wijová M, Moravec F, Horák A, Lukeš J (2006) Evolutionary relationships of Spirurina (Nematoda: Chromadorea: Rhabditida) with special emphasis on dracunculoid nematodes inferred from SSU rRNA gene sequences. Int J Parasitol 36:1067–1075.  https://doi.org/10.1016/j.ijpara.2006.04.005 CrossRefPubMedGoogle Scholar
  26. Wu SG, Wang GT, Xi BW, Gao D, Nie P (2008) Molecular characteristics of Camallanus spp. (Spirurida: Camallanidae) in fishes from China based on its rDNA sequences. J Parasitol 94:731–736.  https://doi.org/10.1645/GE-1219.1 CrossRefPubMedGoogle Scholar
  27. Wu SG, Wang GT, Xi BW, Xiong F, Liu T, Nie P (2009) Population genetic structure of the parasitic nematode Camallanus cotti inferred from DNA sequences of ITS1 rDNA and the mitochondrial COI gene. Vet Parasitol 164:248–256.  https://doi.org/10.1016/j.vetpar.2009.04.030 CrossRefPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Instituto para el Estudio de la Biodiversidad de Invertebrados, Facultad de Ciencias NaturalesUniversidad Nacional de SaltaSaltaArgentina
  2. 2.Programa de Pós-Graduação em Biologia Animal, Instituto de BiociênciasUniversidade Federal de Mato Grosso do SulCampo GrandeBrazil

Personalised recommendations