Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-22T22:13:28.843Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular features of Probopyrus sp. (Isopoda: Bopyridae) from Brazilian Amazonia and the parasitism of inland populations of Macrobrachium amazonicum (Decapoda: Palaemonidae)

Published online by Cambridge University Press:  28 September 2021

Rosa Ilana dos Santos Pereira ,
Cristiana Ramalho Maciel  and
Gabriel Iketani Open the ORCID record for Gabriel Iketani [Opens in a new window]
Rosa Ilana dos Santos Pereira
Affiliation:
Laboratório de Educação e Evolução Prof. Horacio Schneider, Instituto de Ciências da Educação, Universidade Federal do Oeste do Pará – UFOPA, Av. Marechal Rondon, S/N, CEP 68040-070, Santarém, PA, Brasil
Cristiana Ramalho Maciel
Affiliation:
Laboratório de Aqüicultura, Instituto de Estudos Costeiros – IECOS, Universidade Federal do Pará – UFPA, Campus de Bragança, Alameda Leandro Ribeiro, S/N, Aldeia, CEP 68600-000, Bragança, PA, Brasil
Gabriel Iketani*
Affiliation:
Laboratório de Educação e Evolução Prof. Horacio Schneider, Instituto de Ciências da Educação, Universidade Federal do Oeste do Pará – UFOPA, Av. Marechal Rondon, S/N, CEP 68040-070, Santarém, PA, Brasil
*
Author for correspondence: Gabriel Iketani, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Bopyrid isopods of the genus Probopyrus are well-known parasites of freshwater prawns of the genus Macrobrachium. The parasitism of coastal populations of Macrobrachium amazonicum by Probopyrus bithynis, for example, has been documented since the late 1980s. Despite this, molecular data on different populations are not available for any Probopyrus species. The present study is the first to describe Probopyrus populations from distinct regions of the Amazon basin based on sequences of two genes, the mitochondrial cytochrome oxidase C subunit I (COI) and the nuclear 18S ribosomal DNA (18S rDNA) gene. The analyses indicated the presence of two Probopyrus species, each parasitizing either the coastal or the inland populations of M. amazonicum. The results indicated the potential use of the COI barcode for the identification of Probopyrus species. We discuss the potential implications of the findings for the taxonomy of Probopyrus bithynis and other species of the genus Probopyrus.

Keywords

Amazon river prawnCOIDNA sequencenew species18S rDNA
Type
Research Article
Information
Parasitology , Volume 149 , Issue 2 , February 2022 , pp. 203 - 208
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bandelt, H-J, Forster, P and Röhl, A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.10.1093/oxfordjournals.molbev.a026036CrossRefGoogle ScholarPubMed
Beck, JT (1980) The effects of an isopod castrator, Probopyrus pandalicola, on the sex characters of one of its caridean shrimp hosts, Palaemonetes paludosus. The Biological Bulletin 158, 1–15.CrossRefGoogle Scholar
Bialetzki, A, Nakatani, K, Baumgartner, G and Bond-Buckup, G (1997) Occurrence of Macrobrachium amazonicum (Heller) (Decapoda, Palaemonidae) ln Leopoldo's inlet (Ressaco do Leopoldo), upper Paraná river, Porto Rico, Paraná, Brazil. Revista Brasileira de Zoologia 14, 379–390.CrossRefGoogle Scholar
Boyko, CB, Moss, J, Williams, JD and Shields, JD (2013) A molecular phylogeny of Bopyroidea and Cryptoniscoidea (crustacea: Isopoda). Systematics and Biodiversity 11, 495–506.10.1080/14772000.2013.865679CrossRefGoogle Scholar
Brinton, BA and Curran, MC (2015 a) The effect of temperature on synchronization of brood development of the bopyrid isopod parasite Probopyrus pandalicola with molting of its host, the daggerblade grass shrimp Palaemonetes pugio. The Journal of Parasitology 101, 398–404.CrossRefGoogle ScholarPubMed
Brinton, BA and Curran, MC (2015 b) The effects of the parasite Probopyrus pandalicola (Packard, 1879) (Isopoda, Bopyridae) on the behavior, transparent camouflage, and predators of Palaemonetes pugio Holthuis, 1949 (Decapoda, Palaemonidae). Crustaceana 88, 1265–1281.10.1163/15685403-00003501CrossRefGoogle Scholar
Bruford, MW, Hanotte, O, Brookfield, JFY and Burke, T (1998) Multilocus and single-locus DNA fingerprinting. In Hoelzel, AR (ed.), Molecular Genetic Analysis of Populations: A Practical Approach. Oxford, UK: IRL Press, pp. 287–336.Google Scholar
Castro e Silva, SMM and Cavalcante, PPL (1994) Perfil do setor lagosteiro nacional. Brasilia: IBAMA.Google Scholar
Cho, S-M (2012) Development of a denaturing high-performance liquid chromatography (DHPLC) assay to detect parasite infection in grass shrimp Palaemonetes pugio. Fisheries and Aquatic Sciences 15, 107–115.CrossRefGoogle Scholar
Corrêa, LL, Sousa, EMO, Silva, LVF, Adriano, EA, Oliveira, MSB and Tavares-Dias, M (2018) Histopathological alterations in gills of Amazonian shrimp Macrobrachium amazonicum parasitized by isopod Probopyrus bithynis (Bopyridae). Diseases of Aquatic Organisms 129, 117–122.CrossRefGoogle Scholar
Costa, FO, deWaard, JR, Boutillier, J, Ratnasingham, S, Dooh, RT, Hajibabaei, M and Hebert, PDN (2007) Biological identifications through DNA barcodes: the case of the Crustacea. Canadian Journal of Fisheries and Aquatic Sciences 64, 272–295.CrossRefGoogle Scholar
Dale, WE and Anderson, G (1982) Comparison of morphologies of Probopyrus bithynis, P. floridensis, and P. pandalicola larvae reared in culture (Isopoda, Epicaridea). Journal of Crustacean Biology 2, 392–409.CrossRefGoogle Scholar
da Silva, JM, Creer, S, Dos Santos, A, Costa, AC, Cunha, MR, Costa, FO and Carvalho, GR (2011) Systematic and evolutionary insights derived from mtDNA COI barcode diversity in the Decapoda (Crustacea: Malacostraca). Public Library of Science ONE 6, e19449.Google Scholar
de Barros, MSF, da Silva Neto, LS and Calado, TCdS (2021) First record of parasitism by Probopyrus pandalicola (Isopoda, Bopyridae) on the freshwater prawn Macrobrachium acanthurus (Decapoda, Palaemonidae) and ecological interactions. Journal of Parasitic Diseases 45, 273–278.CrossRefGoogle ScholarPubMed
Dreyer, H and Wägele, J-W (2001) Parasites of crustaceans (Isopoda: Bopyridae) evolved from fish parasites: molecular and morphological evidence. Zoology 103, 157–178. doi:0944-2006/01/103/03-04-157Google Scholar
Figueroa, NJ, Figueroa, DF and Hicks, D (2020) Phylogeography of Acartia tonsa Dana, 1849 (Calanoida: Copepoda) and phylogenetic reconstruction of the genus Acartia Dana, 1846. Marine Biodiversity 50, 23.CrossRefGoogle Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Gopalakrishnan, A, Raja, K, Trilles, JP, Rajkumar, M, Rahman, MM and Saravanakumar, A (2017) Bopyrid isopods parasitizing on the cultured fresh water prawn, Macrobrachium malcolmsonii in South India. Journal of Parasitic Diseases 41, 93–96.CrossRefGoogle ScholarPubMed
Hebert, PDN, Cywinska, A, Ball, SL and deWaard, JR (2003) Biological identifications through DNA barcodes. Proceedings of the Biological Sciences/The Royal Society 270, 313–321.CrossRefGoogle ScholarPubMed
Iketani, G, Pimentel, L, Torres, EdS, Rêgo, PSd and Sampaio, I (2021) Mitochondrial heteroplasmy and pseudogenes in the freshwater prawn, Macrobrachium amazonicum (Heller, 1862): DNA barcoding and phylogeographic implications. Mitochondrial DNA Part A 32, 1–11.CrossRefGoogle ScholarPubMed
Kensley, B and Walker, I (1982) Palaemonid shrimps from the Amazon Basin, Brazil (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology 362, 1–28. doi:10.5479/si.00810282.362Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Lefébure, T, Douady, CJ, Gouy, M and Gibert, J (2006) Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution 40, 435–447.CrossRefGoogle ScholarPubMed
Leigh, JW and Bryant, D (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116. doi: 10.1111/2041-210X.12410CrossRefGoogle Scholar
Lemos de Castro, A (1974) Crustaceos isopodos epicarideos do Brasil. IX. Genero Probopyus Giard e Bonnier. Revista Brasileira de Biologia 34, 209–217.Google Scholar
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25, 1451–1452.CrossRefGoogle ScholarPubMed
Maciel, CR and Valenti, WC (2009) Biology, fisheries, and aquaculture of the Amazon River Prawn Macrobrachium amazonicum: a review. Nauplius 17, 61–79.Google Scholar
Markham, JC (1985) A review of the bopyrid isopods infesting caridean shrimps in the northwestern Atlantic Ocean, with special reference to those collected during the Hourglass Cruises in the Gulf of Mexico. Memoirs of the Hourglass Cruises VII, 1–156.Google Scholar
Masunari, S, Da Silva Castagini, A and Oliveira, E (2000) The population structure of Probopyrus floridensis (Isopoda, bopyridae), a parasite of Macrobrachium potiuna (Decapoda, palaemonidae) from the Perequê River, Paranaguá basin, southern Brazil. Crustaceana 73, 1095–1108.Google Scholar
Melo, GAS (2003) Manual de Identificação dos Crustacea Decapoda de Água Doce do Brasil. São Paulo: Loyola.Google Scholar
Odinetz-Collart, O (1988) Aspectos ecológicos do camarão Macrobrachium amazonicum (Heller, 1862) no baixo Tocatins (PA-Brasil). Memoria de la Sociedad de Ciencias Naturales La Salle 48(Suppl), 341–353.Google Scholar
Odinetz-Collart, O (1990) Interactions Entre Le Parasite Probopyrus bithynis (Isopoda, Bopyridae) Et L'Un De Ses Hôtes, La Crevette Macrobrachium Amazonicum (Decapoda, Palaemonidae). Crustaceana 58, 258–269.CrossRefGoogle Scholar
Odinetz-Collart, O (1991) Tucurui dam and the population of the prawn Macrobrachium amazonicum int the Lower Tocantins (Pa-Brazil): a four-year study. Archiv fur Hydrobiology 122, 213–227.CrossRefGoogle Scholar
Odinetz-Collart, O and Moreira, L (1993) Potencial pesqueiro de Macrobrachium amazonicum na Amazônia Central (Ilha do Careiro): variação da abundância e do comprimento. Amazoniana 12, 399–413.Google Scholar
Palumbi, SR and Benzie, J (1991) Large mitochondrial DNA differences between morphologically similar penaeid shrimp. Molecular Marine Biology and Biotechnology 1, 27–34.Google ScholarPubMed
Raupach, MJ and Radulovici, AE (2015) Looking back on a decade of barcoding crustaceans. ZooKeys 2015, 53–81.CrossRefGoogle Scholar
Raupach, MJ, Barco, A, Steinke, D, Beermann, J, Laakmann, S, Mohrbeck, I, Neumann, H, Kihara, TC, Pointner, K, Radulovici, A, Segelken-Voigt, A, Wesse, C and Knebelsberger, T (2015) The application of DNA barcodes for the identification of marine crustaceans from the North Sea and adjacent regions. PLoS One 10, e0139421.CrossRefGoogle ScholarPubMed
Ribeiro, FB, Horch, AP and Williams, JD (2019) New occurrences and host records for two species of parasitic isopods (Isopoda, Cymothoida, Bopyridae) associated with caridean shrimps (Decapoda, Caridea) from Brazil. Journal of Natural History 53, 2437–2447.CrossRefGoogle Scholar
Román-Contreras, R (2004) The genus Probopyrus Giard and Bonnier, 1888 (Crustacea: Isopoda: Bopyridae) in the eastern Pacific with seven new records for Mexico. Contribuciones al Estudio de los Crustáceos del Pacífico Este 3, 153–168.Google Scholar
Saito, N, Shokita, S and Naruse, T (2010) A new species of freshwater bopyrid, Probopyrus iriomotensis (Crustacea: Isopoda), parasitizing Macrobrachium spp.(Crustacea: Decapoda), from Iriomote Island, Ryukyu Islands, Southwestern Japan. Species Diversity 15, 169–183.CrossRefGoogle Scholar
Sampaio, CMS, Silva, RR, Santos, JA and Sales, SP (2007) Reproductive cycle of Macrobrachium amazonicum females (Crustacea, Palaemonidae). Brazilian Journal of Biology 67, 551–559.CrossRefGoogle Scholar
Valencia, DM and Campos, MR (2007) Freshwater prawns of the genus Macrobrachium Bate, 1868 (Crustacea: Decapoda: palaemonidae) of Colombia. Zootaxa 1456, 1–44.CrossRefGoogle Scholar
Vergamini, FG, Pileggi, LG and Mantelatto, FL (2011) Genetic variability of the Amazon River prawn Macrobrachium amazonicum (Decapoda, Caridea, Palaemonidae). Contributions to Zoology 80, 67–83.CrossRefGoogle Scholar
Whiting, MF, Carpenter, JC, Wheeler, QD and Wheeler, WC (1997) The strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 46, 1–68.Google ScholarPubMed
Williams, JD and Boyko, CB (2012) The global diversity of parasitic isopods associated with crustacean hosts (Isopoda: Bopyroidea and Cryptoniscoidea). PLoS One 7, e35350.CrossRefGoogle Scholar
WoRMS Editorial Board (2021) World Register of Marine Species. Available from https://www.marinespecies.org at VLIZ (accessed 2021-07-01). doi:10.14284/170CrossRefGoogle Scholar
Wu, S, Xiong, J and Yu, Y (2015) Taxonomic resolutions based on 18S rRNA genes: a case study of subclass Copepoda. PLoS One 10, e0131498.CrossRefGoogle ScholarPubMed