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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


Newly collected specimens of Procamallanus (Spirocamallanus) macaensis Vicente & Santos, 1972 from the intestine of Paralonchurus brasiliensis (Steindachner), off Rio de Janeiro, Brazil, are redescribed and genetically characterised. Additionally, all congeners deposited in the Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC) parasitic in marine fishes of the South Atlantic, including types of P. (S.) macaensis, were re-evaluated. The following features are described for the first time in P. (S.) macaensis: morphology and arrangement of cephalic structures, shape of deirids and location of phasmids. The position of the excretory pore, the number and arrangement of caudal papillae in males, the structure of the spicules and of tail end in both males and females are rectified. Most specimens deposited in the CHIOC identified as P. (S.) pereirai Annereaux, 1946 were transferred to P. (S.) macaensis and others were designated as Procamallanus (S.) sp. Procamallanus (S.) cruzi Guimarães, Cristófaro & Rodrigues, 1976 is considered a species inquirenda due to its poor description and the lack of match of its original description with the type-material re-examined. Moreover, several taxonomic problems were noted after observations of the specimens (mostly poorly preserved), including inadequate morphological reports as well as misidentifications. Phylogenies inferred using sequences of the SSU rDNA from camallanids (Nematoda: Camallanidae) mostly generated weakly supported clades; however, Camallanus Railliet & Henry, 1915 and Procamallanus Baylis, 1923 do not seem to be monophyletic. Based on the present results and the lack of molecular data, it would be pertinent to adopt the widely-used classification for the subgenera of Procamallanus.

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  1. Anderson, R. C., Chabaud, A. G., & Willmott, S. (2009). Keys to the nematode parasites of vertebrates: archival volume (p. 480). Wallingford: CABI Publishing.

  2. Annereaux, R. F. (1946). A new nematode, Procamallanus pereirai, with a key to the genus. Transactions of the American Microscopical Society, 65, 299–303.

  3. Bashirullah, A. K. M. (1977). Two new camallanid nematodes from marine fishes of Venezuela. Universidad Nacional Autonoma de Mexico Instituto de Biologia Publicaciones Especiales, 4, 391–400.

  4. Bashirullah, A. K. M., & Williams, E. H. (1980). Five new species of the genus Spirocamallanus Olsen, 1952 (Camallanidae, Nematoda) from marine fishes. Journal of Helminthology, 54, 247–252.

  5. Cárdenas, M. Q., & Lanfredi, R. M. (2005). Further description of Procamallanus (Spirocamallanus) halitrophus comb. n. (Nematoda: Camallanidae) from flounder off the Brazilian coast by light and scanning electron microscopy. Journal Parasitology, 91, 606–613.

  6. 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 Parasitologica, 58, 135–148.

  7. 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. Molecular Biology and Evolution, 31, 1625–1637.

  8. Chaudhary, A., Verma, C., Tomar, V., & Singh, V. (2017). Procamallanus spiculogubernaculus Agarwal, 1958 (Nematoda: Camallanidae) from stinging catfish, Heteropneustes fossilis in India: morphological characterization and molecular data. Helminthologia, 54, 1–9.

  9. Choudhury, A., & Nadler, S. A. (2016). Phylogenetic relationships of Cucullanidae (Nematoda) with observations on Seuratoidea and the monophyly of Cucullanus, Dichelyne and Truttaedacnitis. Journal of Parasitology, 102, 87–93.

  10. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.

  11. Froese, R., & Pauly, D. (Eds) (2016). FishBase. World Wide Web electronic publication. http://www.fishbase.org, version 01/2017.

  12. Fusco, A. C., & Overstreet, R. M. (1978). Spirocamallanus cricotus sp. n. and S. halitrophus sp. n. (Nematoda: Camallanidae) from fishes in the northern Gulf of Mexico. Journal of Parasitology, 64, 239–244.

  13. González-Solís, D., Moravec, F., & Vidal-Martínez, V. M. (2002). Procamallanus (Spirocamallanus) chetumalensis n. sp. (Nematoda: Camallanidae) from the mayan sea catfish, Ariopsis similis, off the Caribbean coast of México. Journal of Parasitology, 88, 765–768.

  14. Guerrero, R. (1971). Helmintos de la Hacienda “El Limon”, D. F., Venezuela. Nematodes de vertebrados I. Memorias de la Sociedad de Ciencias Naturales La Salle, 31, 175–230.

  15. Guimarães, J. F., Cristófaro, R., & Rodrigues, H. O. (1976). Alguns nematódeos de peixes de Salvador, Bahia. Atas da Sociedade de Biologia do Rio de Janeiro, 18, 21–25.

  16. Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.

  17. Gupta, N. K., & Garg, V. K. (1986). Studies on the nematode parasites of the genus Spirocamallanus Olsen, 1952 from fish hosts. Part II. Rivista di Parassitologia, 3, 59–83.

  18. Huelsenbeck, J. P., & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.

  19. Katoh, K., Misawa, K., Kuma, K., & Myiata, T. (2002). MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.

  20. Knoff, M., Clemente, S. C., Pinto, R. M., & Gomes, D. C. (2001). Nematodes of elasmobranch fishes from the southern coast of Brazil. Memórias do Instituto Oswaldo Cruz, 96, 81–87.

  21. Kuzmin, Y., Tkach, V. V., Snyder, S. D., & Bell, J. A. (2011). Camallanus Railliet et Henry, 1915 (Nematoda, Camallanidae) from Australian freshwater turtles with descriptions of two new species and molecular differentiation of known. Acta Parasitologica, 56, 213–226.

  22. Luque, J. L., Aguiar, J. C., Vieira, F. M., Gibson, D. I., & Santos, C. P. (2011). Checklist of Nematoda associated with the fishes of Brazil. Zootaxa, 3082, 1–88.

  23. Moravec, F., Justine, J. L., Würtz, J., Taraschewski, H., & Sasal, P. (2006). A new species of Procamallanus (Nematoda: Camallanidae) from Pacific eels (Anguilla spp). Journal of Parasitology, 92, 130–137.

  24. Moravec, F., Salgado-Maldonado, G., & Caspeta-Mandujano, J. M. (2000). Three new Procamallanus (Spirocamallanus) species from freshwater fishes in Mexico. Journal of Parasitology, 86, 119–127.

  25. Moravec, F., & Sey, O. (1988). Nematodes of freshwater fishes from North Vietnam. Part 1. Camallanoidea and Habronematoidea. Acta Societatis Zoologicae Bohemoslovacae, 52, 128–148.

  26. Moravec, F., & Thatcher, V. E. (1997). Procamallanus (Denticamallanus subgen. n.) dentatus n. sp. (Nematoda: Camallanidae) from the characid fish, Bryconops alburnoides, in the Brazilian Amazon. Parasite, 4, 239–243.

  27. Moravec, F., & Van As, L. L. (2015). Procamallanus (Spirocamallanus) spp. (Nematoda: Camallanidae) from fishes of the Okavango River, Botswana, including P. (S.) serranochromis n. sp. parasitic in Serranochromis spp. (Cichlidae). Systematic Parasitology, 90, 151–164.

  28. Nadler, S. A., Carreno, R. A., Mejía-Madrid, H., Ullberg, J., Pagan, C., Houston, R., et al. (2007). Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology, 134, 1421–1443.

  29. Pereira, F. B., & Luque, J. L. (2016). Morphological and molecular characterization of cucullanid nematodes including Cucullanus opisthoporus in freshwater fish from the Brazilian Amazon. Journal of Helminthology. doi:10.1017/S0022149X16000729.

  30. Petter, A.-J. (1979). Essai de classification de la sousfamille des Procamallaninae (Nematoda, Camallanidae). Bulletin du Museum National d’Histoire Naturelle, 1, 991–1008.

  31. Petter, A.-J., Golvan, Y. J., & Tcheprakoff, R. (1977). Nématodes de poissons de rivière en Guadeloupe. Bulletin du Museum National d’Histoire Naturelle, 3, 159–171.

  32. Pinto, R. M., & Noronha, D. (1976). Procamallanus brasileiros (Nematoda, Camallanoidea): considerações finais com chave para determinação das espécies. Memórias do Instituto Oswaldo Cruz, 74, 323–339.

  33. Pinto, R. M., Vicente, J. J., & Noronha, D. (1984). First report of Ascarophis Van Beneden, 1871: A. brasiliensis n.sp. (Nematoda, Ascarophodinae) and Procamallanus (Spirocamallanus) pererai Annereaux, 1946 (Nematoda, Procamallaninae) in South America. Memórias do Instituto Oswaldo Cruz, 79, 491–494.

  34. Rigby, M. C., & Adamson, M. L. (1977). Spirocamallanus species of French Polynesian coral reef fishes. Canadian Journal of Zoology, 75, 1270–1279.

  35. Santos, C. P., Cárdenas, M. Q., & Lent, H. (1999). Studies on Procamallanus (Spirocamallanus) pereirai Annereaux, 1946 (Nematoda: Camallanidae), with new host records and new morphological data on the larval stages. Memórias do Instituto Oswaldo Cruz, 94, 635–640.

  36. Vicente, J. J., & Santos, E. (1972). Sobre um novo nematódeo camalanídeo, parasito de peixe, marinho (Nematoda, Camallanoidea). Atas da Sociedade de Biologia do Rio de Janeiro, 15, 145–147.

  37. Werle, E., Schneider, C., Renner, M., Völker, M., & Fiehn, W. (1994). Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research, 22, 4354–4355.

  38. Wu, S. G., Wang, G. T., Xi, B. W., Gao, D., & Nie, P. (2008). Molecular characteristics of Camallanus spp. (Spirurida: Camallanidae) in fishes from China based on its rDNA sequences. Journal of Parasitology, 94, 731–736.

  39. Yooyen, T., Moravec, F., & Wongsawad, C. (2011). Two new sibling species of Procamallanus (Spirocamallanus) (Nematoda: Camallanidae) from marine fishes in the Gulf of Thailand. Journal of Parasitology, 97, 931–938.

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The authors are thankful to Tomáš Scholz from the Institute of Parasitology, Biology Centre of the Czech Academy of Sciences (IPCAS) and the Staff of the Laboratory of Electron Microscopy from the same institute (IPCAS; RVO: 60077344) and the Czech Science Foundation (project No. P505/12/G112) for the support and for covering costs of SEM observations at the IPCAS. Thanks are also due to Dr. Marcelo Knoff curator of the Coleção Helmintológica do Instituto Oswaldo Cruz (acronym CHIOC) and Daniela A. Lopes by the loan of the specimens analysed in the present study.


Carla J. Sardella was supported by a Master fellowship from CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico do Brasil), Felipe B. Pereira was supported by a PNPD-CAPES Post-doctoral fellowship (Programa Nacional de Pós-Doutorado-Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES, Brazil) and José L. Luque was supported by a Research fellowship from CNPq.

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Correspondence to José L. Luque.

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This article was registered in the Official Register of Zoological Nomenclature (ZooBank) as 13AFF550-ADC0-41B4-842E-B345DB51F877. This article was published as an Online First article on the online publication date shown on this page. The article should be cited by using the doi number. This is the Version of Record.

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Sardella, C.J., Pereira, F.B. & Luque, J.L. 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 (2017). https://doi.org/10.1007/s11230-017-9728-2

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  • Excretory Pore
  • Anterior Extremity
  • Basal Ring
  • Buccal Capsule
  • Muscular Oesophagus