Abstract
Mullets (Mugilidae) are economically-important fish exploited extensively by artisanal fisheries on the Amazon coast of Brazil. In the present study, 150 specimens of redeye mullet (Mugil rubrioculus) acquired from the public fish market were examined, and the gill filaments of 90 (60%) were found to be infected with spores of Myxobolus. The mature spores were spherical, with a mean diameter of 6.28±0.33 μm, and had polar capsules of equal size (2.47±0.34 μm in length and 1.58±0.27 μm in width). The 18S rRNA sequence of the parasite was compared with those of other myxosporidian species available in the GenBank database. The morphological and molecular characteristics of the parasite indicate strongly the existence of a new species, denominated Myxobolus bragantinus n. sp., the first case of a new myxosporidian species to be found in this host. [Zoobank: urn:lsid:zoobank.org:act:E00F72E1-9302-423F-BA4E-51C05D0770C8]
References
Bahri, S., Andree, K.B. & Hedrick, R.P. (2003) Morphological and phylogenetics of marine Myxobolus spp. from Mullet in Icheul Lake, Tunisia. Journal of Eukaryotic Microbiology, 50, 463–470.
https://doi.org/10.1111/j.1550-7408.2003.tb00272.x
Boreham, R.E., Hendrick, S., O’Donoghue, P.J. & Stenzel, D.J. (1998) Incidental finding of Myxobolus spores (Protozoa: Myxozoa) in stool samples from patients with gastrointestinal symptoms. Journal of Clinical Microbiology, 36 (12), 3728–3730. Available from: http://jcm.asm.org/content/36/12/3728.full.pdf+html (accessed 5 January 2018).
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83(4), 575−583.
https://doi.org/10.2307/3284227Cerqueira VR (2004) Cultivo de peixes marinhos. In: Poli CR, Poli ATB, Andreatta ER, Beltrame E, (Eds.) Aqüicultura: Experiências Brasileiras. Multitarefa, Florianópolis, SC, pp.369–406.
Cervigón, F., Capriani, F., Fischer, W., Garibaldi, L., Hendrickx, M., Lemus, A.J., Márquez, R., Poutiers, J.M., Robaina, G. & Rodriguez, B. (1993) FAO species identification sheets for fishery purposes. Field guide to the commercial marine and brackishwater resources of the northern coast of South America, Rome FAO, pp. 513.
Chen, Q.L. & Ma, C.L. (1998) Myxozoa, Myxosporea. Fauna Sinica. Beijing, Science Press, pp. 292–528
Dar, S.A., Kaur, H. & Chishti, M.Z. (2017) Myxobolus chushi n. sp. (Myxozoa:Myxosporea) parasitizing Schizothorax niger (Heckel), a native cyprinid fish fromWullar Lake in Kashmir Himalayas. Parasitology International, 66, 272–278.
https://doi.org/10.1016/j.parint.2017.02.004
Eiras, J.C., Abreu, P.C., Robaldo, R. & Pereira Júnior, J. (2007) Myxobolus platanus n. sp. (Myxosporea, Myxobolidae), a parasite of Mugil platanus Günther, 1880 (Osteichthyes, Mugilidae) from Lagoa dos Patos, RS, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 59 (4), 895–898.
https://doi.org/10.1590/S0102-09352007000400012
Eiras, J.C. & D'Souza, J. (2004) Myxobolus Goensis n. sp. (Myxozoa, Myxosporea, Myxobolidae), a Parasite of the Gills of Mugil Cephalus (Osteichthyes, Mugilidae) From Goa, India. Parasite, 11, 243–248.
https://doi.org/10.1051/parasite/2004113243
Eiras, J.C., Zhang, J. & Molnar, K. (2014) Synopsis of the species of Myxobolus Butschli, 1882 (Myxozoa: Myxomyxosporea, Myxobolidae) described between 2005 and 2013. Systematic Parasitology, 88, 11–36.
https://doi.org/10.1007/s11230-014-9484-5
Espírito Santo, R.V., Isaac, V.J., Silva, L.M.A., Martinelli, J.M., Higuchi, H. & Saint-Paul, U. (2005) Peixes e camarões do litoral bragantino, Pará, Brasil. MADAM, Belém, pp. 268.
Ferguson, J.A., Atkinson, S.D., Whipps, C.M. & Kent, M.L. (2008) Molecular and morphological analysis of Myxobolus spp. of salmonid fishes with the description of Myxobolus fryeri n. sp. Journal of Parasitology, 94, 1322–1334.
https://doi.org/10.1645/GE-1606.1
Fiala, I. (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology, 36, 1521–1534.
https://doi.org/10.1016/j.ijpara.2006.06.016
Fiala, I., Bartošová P.S. & Whipps, C.M. (2015) Classification and Phylogenetics of Myxozoa. In: Okamura, B., Gruhl, A. & Bartholomew, J. (Eds.) Myxozoan Evolution, Ecology and Development, pp. 85–110.
https://doi.org/10.1007/978-3-319-14753-6_5
Freire, J.L., Bentes, B.S. & Souza, A.S. (2011) Aspectos econômicos e higiênico sanitário da comercialização do pescado no Município de Bragança (PA). Biota Amazônia, 1(2), 17–28, 2011.
https://doi.org/10.18561/2179-5746/biotaamazonia.v1n2p17-28
Froese, R. & Pauly, D. (2016) FishBase. FishBase Information and Research Group, Inc. Available from: http://www.fishbase.org (accessed 15 Dezembre 2017)
Guindon, S. & Gascuel, O. (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.
https://doi.org/10.1080/10635150390235520
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symposium Series, 41, 95–98. Available from: http://brownlab.mbio.ncsu.edu/JWB/papers/1999Hall1.pdf (accessed 5 January 2018)
Harrison, I.J. (2003) Mugilidae,. In: Carpenter, K.E. (Eds.), The living marine resources of the Western Central Atlantic. Vol. 2. FAO species identification guide for fihery purpose, pp. 1071–1085.
Harrison, I.J., Nirchio, M., Oliveira, C., Ron, E. & Gaviria, J. (2007) A new species of mullet (Teleostei: Mugilidae) from Venezuela, with a discussion on the taxonomy of Mugil gaimardianus. Journal of Fish Biology, 71 (Supplement A), 76–97.
https://doi.org/10.1111/j.1095-8649.2007.01520.x.
Kaur, H., Attri, R. (2015) Prevalence and tissue specificity of Myxobolus saugati Kaur and Singh, 2011 (Myxozoa; Myxosporea; Bivalvulida) causing dermal myxoboliosis in wild and cultured Indian major carps in Punjab. Species, 15, 14–18. Available from: http://www.discovery.org.in (accessed 15 Dezembre 2017)
Kaur, H. & Katoch, A. (2016) Prevalence, site and tissue preference of myxozoan parasites infecting gills of cultured fish in Punjab (India). Diseases of Aquatic Organisms, 118, 129–137.
https://doi.org/10.3354/dao02959
Kaur, H. & Singh, R. (2008) Observations on one new species of genus Myxobolus–M. naini and redescription of M. magauddi recorded from freshwater fishes of Kanjali Wetland of Punjab, India. In: Proceedings of 20th National Congress Parasitology, NEHU, Shillong, India, pp. 75–79.
Kent, M.L., Andree, K.B., Bartholomew, J.L., El-Matbouli, M., Desser, S.S., Devlin, R.H., Feist, S.W., Hedrick, R.P., Hoffmann, R.W., Khattra, J., Hallett, S.L., Lester, R.J.G., Longshaw, M., Palenzeula, O., Siddall, M.E. & Xiao, C. (2001) Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology, 48 (4), 395–413.
https://doi.org/10.1111/j.1550-7408.2001.tb00173.x.
Kim, W.S., Kim, J.H. & Oh, M.J. (2013) Morphologic and Genetic Evidence for Mixed Infection with Two Myxobolus Species (Myxozoa: Myxobolidae) in Gray Mullets, Mugil cephalus, from Korean Waters. Korean Journal of Parasitology, 51 (3), 369–373.
https://doi.org/10.3347/kjp.2013.51.3.369
Kim, W.S., Kim, J.H., Jang, M.S., Jung, S.J. & Oh, M.J. (2013) Infection of wild mullet (Mugil cephalus) with Myxobolus episquamalis in Korea. Parasitology Research, 112, 447–451.
https://doi.org/10.1007/s00436-012-3075-7
Liu, X., Hua, C., Zhang, Q., Zhao, Y., Zhang, D. & Zhang, J. (2017) Myxobolus taibaiensis sp. n. (Myxozoa: Myxosporea) infecting the intestinal wall of common carp Cyprinus carpio Linnaeus in China. Folia Parasitologica, 64, 1–7.
https://doi.org/001-007.10.14411/fp.2017.001
Liu, Y., Whipps C.M., Gu, Z.M., Huang, M.J., He, C., Yang, H.L. & Molnár, K. (2013) Myxobolus musseliusae (Myxozoa: Myxobolidae) from the gills of common carp Cyprinus carpio and revision of Myxobolus dispar recorded in China. Parasitology Research, 112, 289–296.
https://doi.org/10.1007/s00436-012-3136-y
Liu, Y., Whipps C.M., Gu, Z.M. & Zeng, L.B. (2010) Myxobolus turpisrotundus (Myxosporea: Bivalvulida) spores with caudal appendages: investigating the validity of the genus Henneguya with morphological and molecular evidence. Parasitology Research, 107, 699–706.
https://doi.org/10.1007/s00436-010-1924-9
Lom, J. & Arthur, J.R. (1989) A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases, 12 (2), 151–156.
https://doi.org/10.1111/j.1365-2761.1989.tb00287.x
Lom, J. & Diková, I. (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica (Praha), 53 (1), 1–36.
http://dx.doi.org/10.14411/fp.2006.001
Luna L.G. (1968) Manual of histologic staining methods of the armed forces institute of pathology. MacGraw-Hill Book Company, New York, pp. 258.
Marceniuk, A.P., Caires, R.A., Rotundo, M.M., De Alcântara, R.A.K. & Wosiacki, W.B. (2017) The icthyofauna (Teleostei) of the Rio Caeté estuary, northeast Pará, Brazil, with a species identification key from northern Brazilian coast. Pan-American Journal of Aquatic Sciences, 12 (1), 31–79. Available from: http://www.panamjas.org/pdf_artigos/PANAMJAS_12(1)_31-79.pdf (accessed 15 Dezembre 2017)
Marcotegui, P. & Martorelli, S. (2017) Myxobolus saladensis sp. nov., a new species of gill parasite of Mugil liza (Osteichthyes, Mugilidae) from Samborombón Bay, Buenos Aires, Argentina. Iheringia, Série Zoologia, 107, 1–5.
https://doi.org/10.1590/1678-4766e2017026
McClelland, R.S., Murphy, D.M. & Cone, D.K. (1997) Report of spores of Henneguya salminicola (Myxozoa) in human stool specimens: possible source of confusion with human spermatozoa. Journal of Clinical Microbiology, 35 (11), 2815–2818. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC230068/pdf/352815.pdf (accessed 5 January 2018)
Medeiros Junior, E.F., Eiras, B.J.C.F., Rodrigues, E.C. & Alves, M.M. (2015) Avaliação higiênico-sanitária do pescado comercializado na cidade de Bragança Pará. Nutritime, 12(5), 4237–4243. Available from: http://www.nutritime.com.br/arquivos_internos/artigos/323_-_4237-4243_-_NRE_12-5_set-out_2015.pdf (accessed 5 January 2018)
Menezes, N.A. (1983) Guia prático para o conhecimento e identificação das tainhas e paratis (Pisces: Mugilidae) do litoral brasileiro. Revista Brasileira de Zoologia, 2 (1), 1–12.
https://doi.org/10.1590/S0101-81751983000100001
Menezes, N.A., Buckup, P.A., Figueiredo, J.L., Moura, R.L. (2003). Catálogo das espécies de peixes marinhos do Brasil. Museu de Zoologia Universidade de São Paulo, São Paulo, pp. 164.
Menezes, N.A., Nirchio, M., De Oliveira, C., & Siccharamirez, R. (2015) Taxonomic review of the species of Mugil (Teleostei: Perciformes: Mugilidae) from the Atlantic South Caribbean and South America, with integration of morphological, cytogenetic and molecular data. Zootaxa, 3918(1), 1–38.
https://doi.org/10.11646/zootaxa.3918.1.1
Milanin, T., Eiras,J.C., Arana, S., Maia, A.A.M., Alves, A.L., Silva, M.R.M., Carriero, M.M., Ceccarelli, P.S. & Adriano, E.A. (2010) Phylogeny, ultrastructure, histopathology and prevalence of Myxobolus oliveirai sp. nov., a parasite of Brycon hilarii (Characidae) in the Pantanal wetland, Brazil. Memórias do Instituto Oswaldo Cruz, 105 (6), 762–769.
https://doi.org/10.1590/S0074-02762010000600006
Molnár K. (2002) Site preference of fish myxosporeans in the gill. Diseases Of Aquatic Organisms, 48, 197–207.
https://doi.org/10.3354/dao048197
Molnár, K., Eszterbauer, E., Székely, C. & Harrach, B. (2002) Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. Journal of Fish Diseases, 25 (11), 643–652.
https://doi.org/10.1046/j.1365-2761.2002.00409.x
Moncada, L.I., López, M.C., Murcia, M.I., Nicholls, S., León, F., Guío, O.L. & Corredor, A. (2001) Myxobolus sp., another opportunistic parasite in immunosuppressed patients. Journal of Clinical Microbiology, 39(5), 1938–1940.
https://doi.org/10.1128/JCM.39.5.1938-1940.2001
Naldoni, J., Zatti, S.A., Capodifoglio, K.R.H., Milanin, T., Maia, A.A.M., Silva, M.R.M. & Adriano, E.A. (2015) Host-parasite and phylogenetic relationships of Myxobolus filamentum sp. n. (Myxozoa: Myxosporea), a parasite of Brycon orthotaenia (Characiformes: Bryconidae) in Brazil. Folia Parasitologica, 62, 014–021.
https://doi.org/10.14411/fp.2015.014
Nascimento, M.S., Cardoso, C.A., Fernandes, S.P., Pereira, L.G. & Silva, B.B. (2016) Desembarque e modelo preditivo de produção de tainhas (Mugilidae) em um polo pesqueiro do nordeste amazônico. Biota Amazônia, 6 (2), 80–85.
https://doi.org/10.18561/2179-5746/biotaamazonia.v6n2p80-85
Nelson, J.S. (2006) Fishes of the World, 4 (Ed.). John Wiley and Sons, New York. pp. 601.
Nirchio, M., Oliveira, C., Siccha-Ramirez, Z.R., de Sene, V.F., Sola, L., Milana, V. & Rossi, A.R. (2017) The Mugil curema species complex (Pisces, Mugilidae): a new karyotype for the Pacific white mullet mitochondrial lineage. Comparative Cytogenetics 11(2), 225–237.
https://doi.org/10.3897/CompCytogen.v11i2.11579
Ovcharenko, M. (2015) Microparasites of worldwide mullets. Annals of Parasitology, 61(4), 229–239.
https://doi.org/10.17420/ap6104.12
Özer, A., Gürkanlı, C.T., Özkan, H., Acar, G., Çiftçi, Y. & Yurakhno, V. (2016) Molecular characterization and morphological aspects of Myxobolus parvus (Myxozoa) from Liza saliens (Mugilidae) off the Turkish Black Sea coasts. Parasitology Research, 115(9), 3513–3518.
https://doi.org/10.1007/s00436-016-5115-1
Page, R.D (1996) TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences, 12(4), 357–358.
https://doi.org/10.1093/bioinformatics/12.4.357
Pavanelli, G.C., Eiras, J.C., Takemoto, R.M. (2002) Doenças de peixes: profilaxia, diagnóstico e tratamento. 2. ed., Maringá: Eduem. pp. 305.
Posada, D. (2008) jModel test: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.
https://doi.org/10.1093/molbev/msn083
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 1 9 (12), 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180
Santos, A.F.L. dos, Diniz, D.G., Takemoto, R.M., França, C.C.S. & Fujimoto, R.Y. (2017) Occurrence of Ergasilus versicolor (Copepoda: Ergasilidae) in Mugil gaimardianus (Osteichthyes: Perciformes) from the estuarine area of Bragança, Pará, Brazil. Revista da Biologia, 17(2), 8–11.
https://doi.org/10.7594/revbio.17.02.02
Santos, C.A.M.L. (2017) Doenças parasitárias associadas ao consume de pescado no brasil: incidência e epidemiologia. Higiene Alimentar, 31(270/271), 65–71. Available from: http://docs.bvsalud.org/biblioref/2017/08/848876/270-271-jul-ago-2017-65-71.pdf (accessed 9 february 2018)
Silva. E.S.C., Cunha, D.S., Araújo, C.S.P., Sales, A.D. & Holanda, F.C.A. (2012) Cadeia de comercialização do pescado desembarcado no posto fiscal de Bragança, estado do Pará. Laboratório de Ciências do Mar, 1(45), 82–87. Available from: www.periodicos.ufc.br/arquivosdecienciadomar/article/download/147/147 (accessed 9 february 2018)
Swofford, D.L. (2003) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, Massachusetts.
Thomson, J.M. (1997) The Mugilidae of the world. Memoirs of the Queensland Museum, Vol. 41. South Brisbane, Q., Australia, pp. 457–562.
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., & Higgins, D.G. (1997) The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24, 4876–4882. Available from:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC147148/pdf/254876.pdf (accessed 5 January 2018)
U-Taynapun K, Penprapai N, Bangrak P, Mekata T, Itami T, Tantikitti C (2011) Myxobolus supamattayai n. sp. (Myxosporea:Myxobolidae) from Thailand parasitizing the scale pellicle of wild mullet (Valamugil seheli). Parasitology Research, 109 (1), 81–91.
https://doi.org/10.1007/s00436-010-2223-1
Woo, P.T.K. (2006) Fish Diseases and Disorders: Protozoan and Metazoan Infections. 2. ed. UK: CAB International, Vol.1, pp. 791.
Yurakhno, V.M. & Ovcharenko, M.O. (2014) Study of Myxosporea (Myxozoa), infecting worldwide mullets with description of a new species. Parasitology Research, 113, 3661–3674.
https://doi.org/10.1007/s00436-014-4031-5