Hostname: page-component-77c89778f8-vsgnj Total loading time: 0 Render date: 2024-07-17T17:48:15.892Z Has data issue: false hasContentIssue false
  • English
  • Français

Integrative taxonomy of Urocleidoides spp. (Monogenoidea: Dactylogyridae) parasites of characiform and gymnotiform fishes from the coastal drainages of the Eastern Amazon, Brazil

Published online by Cambridge University Press:  03 August 2023

J.F. Santos Neto Open the ORCID record for J.F. Santos Neto [Opens in a new window]  and
M.V. Domingues Open the ORCID record for M.V. Domingues [Opens in a new window]
J.F. Santos Neto
Affiliation:
Laboratório de Sistemática e Coevolução, Universidade Federal do Pará, Campus Universitário de Bragança, Instituto de Estudos Costeiros, Travessa Leandro Ribeiro, s/n, Aldeia, 68600–000, Bragança, Pará, Brazil Programa de Pós-Graduação em Biologia Ambiental, Universidade Federal do Pará.
M.V. Domingues*
Affiliation:
Laboratório de Sistemática e Coevolução, Universidade Federal do Pará, Campus Universitário de Bragança, Instituto de Estudos Costeiros, Travessa Leandro Ribeiro, s/n, Aldeia, 68600–000, Bragança, Pará, Brazil Programa de Pós-Graduação em Biologia Ambiental, Universidade Federal do Pará.
*
Corresponding author: M.V. Domingues; Email: mvdomingues@ufpa.br
Get access Rights & Permissions [Opens in a new window]

Abstract

Eight species (four new) of Urocleidoides are reported from Characiformes and Gymnotiformes fishes of the coastal drainages of the Eastern Amazon. Urocleidoides vanini n. sp. is characterized by having a male copulatory organ (MCO) with three and a half counterclockwise rings, absence of vaginal sclerite, and a V-shaped ventral bar. Urocleidoides atilaiamarinoi n. sp. has MCO with two and a half counterclockwise rings, dumbbell-shaped accessory piece, similar anchors, open V-shaped ventral bar, and open U-shaped dorsal bar. Urocleidoides macrosoma n. sp. exhibits an elongate and robust body, MCO comprising one counterclockwise ring, similar anchors with wavy point, and dumbbell-shaped ventral and dorsal bars. Urocleidoides nataliapasternakae n. sp. has MCO comprising two and a half counterclockwise rings, vaginal canal convoluted, point of the dorsal anchor with ornamentation as sclerotized shredded filaments, elongate dumbbell-shaped ventral bar, and U-shaped dorsal bar. Urocleidoides naris and Urocleidoides brasiliensis from H. malabaricus (Characiformes) and the incertae sedis species, Urocleidoides gymnotus and Urocleidoides carapus, from Sternopygus macrurus (Gymnotiformes) are reported, and their molecular sequences are presented in this study. Phylogenetic analyses based on molecular data (28S rDNA and COI mtDNA) reveal that species of Urocleidoides lacking vaginal sclerite are closely related to species that possess vaginal sclerite, suggesting that the absence of vaginal sclerite in Urocleidoides may be the result of a secondary loss. The relationships between species of Urocleidoides and other Neotropical dactylogyrids are also addressed.

Keywords

parasitesErythrinidaeHypopomidaeCOI mtDNA28S rDNA
Type
Research Paper
Information
Journal of Helminthology , Volume 97 , 2023 , e64
Copyright
© The Author(s), 2023. 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

Acosta, AA, Franceschini, L, Zago, AC, Scholz, T, and da Silva, RJ (2017) Six new species of Heteropriapulus (Monogenea: Dactylogyridae) from South American fishes with an amended diagnosis to the genus. Zootaxa 4290, 459–482.CrossRefGoogle Scholar
Acosta, AA, Mendoza-Palmero, CA, da Silva, RJ, and Scholz, T (2019) A new genus and four new species of dactylogyrids (Monogenea), gill parasites of pimelodid catfishes (Siluriformes: Pimelodidae) in South America and the reassignment of Urocleidoides megorchis Mizelle et. Kritsky, 1969. Folia Parasitologica 66, 1–12.Google ScholarPubMed
Acosta, AA, Scholz, T, Blasco-Costa, I, Alves, PV, and da Silva, RJ (2018) A new genus and two new species of dactylogyrid monogeneans from gills of Neotropical catfishes (Siluriformes: Doradidae and Loricariidae). Parasitology International 67, 4–12.CrossRefGoogle ScholarPubMed
Boeger, WA and Kritsky, DC (1997) Coevolution of the Monogenoidea (Platyhelminthes) based on a revised hypothesis of parasite phylogeny. International Journal for Parasitology 27(12), 1495–1511.CrossRefGoogle ScholarPubMed
Boeger, WA, Piasecki, W, and Sobecka, E (2002) Neotropical Monogenoidea. 44. Mymarothecium viatorum sp. n. (Ancyrocephalinae) from the gills of Piaractus brachypomus (Serrasalmidae, Teleostei) captured in a warm-water canal of a power plant in Szczecin, Poland. Acta Ichthyologica et Piscatoria 2(32), 157–161.CrossRefGoogle Scholar
Boeger, WA and Vianna, RT (2006) Monogenoidea. pp. 42–116 in Thatcher, VE (Ed), Aquatic biodiversity in Latin America: Amazon fish parasites. Moscow, Pensoft Publishers.Google Scholar
Braga, MP, Razzolini, E, and Boeger, WA (2015) Drivers of parasite sharing among Neotropical freshwater fishes. Journal of Animal Ecology 84, 487–497.CrossRefGoogle ScholarPubMed
Bush, AO, Lafferty, KD, Lotz, JM, and Shostak, W (1997) Parasitology meets ecology on its own terms: Margolis et al. Revisited. Journal Parasitology 83, 575–583.CrossRefGoogle ScholarPubMed
Bychowsky, BE and Nagibina, LF (1977) The systematic position of some representatives of lower monogeneans frommarine fish. Parazitologicheski Sbornik 27, 7–17 (in Russian).Google Scholar
Desdevises, Y, Morand, S, Jousson, O, and Legendre, P (2002) Coevolution between Lamellodiscus (Monogenea, Diplectanidae) and Sparidae (Teleostei): The study of a complex host–parasite system. Evolution 56(12), 2459–2471.Google Scholar
Domingues, MV and Boeger, WA (2008) Phylogeny and revision of Diplectanidae Monticelli, 1903 (Platyhelminthes: Monogenoidea). Zootaxa 1698, 1–40.CrossRefGoogle Scholar
Ferreira, KDC, Rodrigues, ARO, Cunha, JM, and Domingues, MV (2018) Dactylogyrids (Platyhelminthes, Monogenoidea) from the gills of Hopliasmalabaricus (Characiformes: Erythrinidae) from coastal rivers of the Oriental Amazon Basin: species of Urocleidoides and Constrictoanchoratus n. gen.. Journal of Helminthology May;9 2(3):353–368. doi: 10.1017/S0022149X17000384. Epub 2017 May 15. PMID: 28502254.CrossRefGoogle Scholar
Franceschini, L, Zago, AC, Müller, MI, Francisco, CJ, Takemoto, RM, and da Silva, RJ (2017) Morphology and molecular characterization of Demidospermus spirophallus n. sp., D. prolixus n. sp. (Monogenea: Dactylogyridae) and a redescription of D. anus in siluriform catfish from Brazil. Journal of Helminthology 92, 228 – 243.CrossRefGoogle Scholar
Franceschini, L, Acosta, AA, Zago, AA, Müller, MI, and da Silva, RJ (2020) Trinigyrus spp. (Monogenea: Dactylogyridae) from Brazilian catfishes: New species, molecular data and new morphological contributions to the genus. Journal of Helminthology 94, e126, 1–15.CrossRefGoogle ScholarPubMed
Freitas, AJB, Bezerra, CAM, Meneses, YC, Justo, MCN, Viana, DC, and Cohen, SC (2021) Three new species of Urocleidoides (Monogenoidea: Dactylogyridae) parasitizing characiforms (Actinopterygii: Characiformes) in Tocantins River, states of Tocantins and Maranhão, and new record for U. triangulus in Guandu River, state of Rio de Janeiro, Brazil. Zoologia 38, 1–11.CrossRefGoogle Scholar
Gasques, LS, Graça, RJ, Prioli, SM, Takemoto, RM, and Prioli, AJ (2016) Molecular characterization of Urocleidoides cuiabai and U. malabaricusi (Monogenea: Dactylogyridae) from the trahira fish Hoplias aff. malabaricus in the Paraná River, Brazil. Journal Helminthology 90, 693–697.CrossRefGoogle ScholarPubMed
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W, and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.CrossRefGoogle ScholarPubMed
Humason, GL (1979) Animal tissue techniques. San Francisco, USA, W. H. Freeman. 661 pp.Google Scholar
Jogunoori, W, Kritsky, DC, and Venkaranarasaiah, J (2004) Neotropical Monogenoidea. 46. Three new species from the gills of introduced aquarium fishes in India, the proposal of Heterotylus n. g. and Diaphorocleidus n. g., and the reassignment of some previously described species of Urocleidoides Mizelle & Price, 1964 (Polyonchoinea: Dactylogyridae). Systematic Parasitology 58, 115–124.CrossRefGoogle Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Mentjies, P, and Drummond, A (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.CrossRefGoogle ScholarPubMed
Kmentová, N, Cruz-Laufer, AJ, Pariselle, A, Smeets, K, Artois, T, and Vanhove, MPM (2022) Dactylogyridae 2022: A meta-analysis of phylogenetic studies and generic diagnoses of parasitic flatworms using published genetic and morphological data. International Journal for Parasitology 52(7), 427–457.CrossRefGoogle ScholarPubMed
Kritsky, DC and Thatcher, VE (1974) Monogenetic trematodes (Monopisthocotylea: Dactylogyridae) from freshwater fishes of Colombia, South America. Journal of Helminthology, 48, 59–66.CrossRefGoogle ScholarPubMed
Kritsky, DC and Thatcher, VE (1983) Neotropical Monogenea. 5. Five new species from aruana, Osteoglossum bicirrisum Vandelli, a freshwater teleost from Brazil, with the proposal of Gonocleithrum n. gen. (Dactylogyridae: Ancyrocephalinae). Proceedings of the Biological Society of Washington 96, 581–597.Google Scholar
Kritsky, DC, Thatcher, VE, and Boeger, WA (1986) Neotropical Monogenea. Revision of Urocleidoides (Dactylogyridae, Ancyrocephalinae). Proceedings of the Helminthological Society of Washington 53, 1–37.Google Scholar
Kritsky, DC, Thatcher, VE, and Boeger, WA (1989) Neotropical Monogenea. 15. Dactylogyrids from the gills of Brazilian Cichlidae with proposal of Sciadicleithrum gen. n. (Dactylogyridae). Proceeding of the Helminthological Society of Washington 56, 128–140.Google Scholar
Kritsky, DC, Mendoza-Franco, EF, and Scholz, T (2000) Neotropical Monogenoidea. 36. Dactylogyrids from the gills of Rhamdia guatemalensis (Siluriformes: Pimelodidae) from cenotes of the Yucatan Peninsula, Mexico, with proposal of Ameloblastella gen. n. and Aphanoblastella gen. n. (Dactylogyridae: Ancyrocephalinae). Journal of the Helminthological Society of Washington 67(1), 76–84.Google Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C, and Tamura, K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Littlewood, DTJ and Olson, PD (2001) SSU rDNA and the Platyhelminthes: Signal, noise, conflict and compromise. pp. 262–278 in Littlewood, DTJ and Bray, RA (Eds), Interrelationships of the platyhelminthes. London, UK, Taylor & Francis.Google Scholar
Luque, JL and Iannacone, J (1991) Rhamnocercidae (Monogenea: Dactylogyroidea) in Sciaenidae fishes from Perú, withdescription of Rhamnocercoides menticirrhi n. gen., n. sp. and two new species of Rhamnocercus. Revista de BiologiaTropical 39, 193–201.Google Scholar
Mendoza-Franco, EF and Reina, RG (2008) Five new species of Urocleidoides (Monogenoidea) (Mizelle and price 1964) Kritsky, Thatcher, and Boeger, 1986 parasitizing the gills of Panamanian freshwater fishes. Journal of Parasitology 94(4), 793–802.CrossRefGoogle ScholarPubMed
Mendoza-Franco, EF, Aguirre-Macedo, ML, and Vidal-MartÍnez, VM (2007) New and previously described species of Dactylogyridae (Monogenoidea) from the gills of Panamanian freshwater fishes (Teleostei). The Journal of Parasitology 93(4), 761–771.CrossRefGoogle ScholarPubMed
Mendoza-Franco, EF, Mendoza-Palmero, CA, and Scholz, T (2016) New species of Ameloblastella Kritsky, Mendoza-Franco & Scholz, 2000 and Cosmetocleithrum Kritsky, Thatcher & Boeger, 1986 (Monogenea: Dactylogyridae) infecting the gills of catfishes (Siluriformes) from the Peruvian Amazonia. Systematic Parasitology 93(9), 847–862.CrossRefGoogle ScholarPubMed
Mendoza-Franco, EF, Posel, P, and Dumailo, S (2003) Monogeneans (Dactylogyridae: Ancyrocephalinae) of freshwater fishes from the Caribbean coast of Nicaragua. Comparative Parasitology 70, 32–41.CrossRefGoogle Scholar
Mendoza-Franco, EF, Reina, RG, and Torchin, ME (2009) Dactylogyrids (Monogenoidea) parasitizing the gills of Astyanax spp. (Characidae) from Panama and Southeast Mexico, a new species of Diaphorocleidus and a proposal for Characithecium n. gen. Journal Parasitology 95, 46–55.CrossRefGoogle Scholar
Mendoza-Franco, EF, Caspeta-Mandujano, JM, Salgado-Maldonado, G, and Matamoros, WA (2015) Two new species of Urocleidoides Mizelle et Price, 1964 (Monogenoidea) from the gill lamellae of profundulids and poeciliids from Central America and southern Mexico. Folia Parasitologica 62, 1–7.CrossRefGoogle Scholar
Mendoza-Palmero, CA and Scholz, T (2011) New species of Demidospermus (Monogenea: Dactylogyridae) of pimelodid catfish (Siluriformes) from Peruvian Amazonia and the reassignment of Urocleidoides lebedevi Kritsky and Thatcher, 1976. Journal Parasitology 97(4), 586–592.CrossRefGoogle ScholarPubMed
Mendoza-Palmero, CA, Blasco-Costa, I, and Scholz, T (2015) Molecular phylogeny of Neotropical monogeneans (Platyhelminthes: Monogenea) from catfishes (Siluriformes). Parasite & Vector 8, 1–11.CrossRefGoogle ScholarPubMed
Mendoza-Palmero, CA, Mendoza-Franco, EF, Acosta, AA, and Scholz, T (2019) Walteriella n. g. (Monogenoidea: Dactylogyridae) from the gills of pimelodid catfishes (Siluriformes: Pimelodidae) from the Peruvian Amazonia based on morphological and molecular data. Systematic Parasitology 96, 441–452.CrossRefGoogle Scholar
Mizelle, JD and Blatz, V (1941) Studies on monogenetic trematodes VI. Two new dactylogyrid genera from Floridafishes. American Midland Naturalist 26, 105–109.CrossRefGoogle Scholar
Mizelle, JD and Klucka, AR (1953) Studies on monogenetic trematodes. XVI. Dactylogyridae from Wisconsin fishes. American Midland Naturalist 49, 720–733.CrossRefGoogle Scholar
Mizelle, JD and Kritsky, DC (1969) Studies on monogenetic trematodes. XXXIX. Exotic species of Monopithocotylea with the proposal of Archidiplectanum gen. n. and Longihaptor gen. n. American Midland Naturalist 81, 370–386.CrossRefGoogle Scholar
Mizelle, JD and Price, CE (1963) Additional haptoral hooks in the genus Dactylogyrus. Journal of Parasitology 49, 1028–1029.CrossRefGoogle Scholar
Mizelle, JD and Price, CE (1964) Studies on monogenetic trematodes. XXVII. Dactylogyrid species with the proposal of Urocleidoides gen. n. The Journal of Parasitology 50(4), 579–584.CrossRefGoogle ScholarPubMed
Mizelle, JD and Kritsky, DC (1967) Unilatus gen. n., a unique neotropical genus of Monogenea. Journal of Parasitology 53, 1113–1114.CrossRefGoogle Scholar
Mizelle, JD, Kritsky, DC, and Crane, JW (1968) Studies on monogenetic trematodes. XXXVIII. Ancyrocephalinae from South America with the proposal of Jainus gen. n. American Midland Naturalist 80, 186–198.CrossRefGoogle Scholar
Molmar, K, Hanek, G, Fernando, CH (1974) Ancyrocephalids (Monogenea) from freshwater fishes of Trinidad. The Journal of Parasitology, 60(6), 914–920.CrossRefGoogle Scholar
Monaco, HL, Wood, RA, and Mizelle, JD (1954) Studies on monogenetic trematodes. XVI. Rhamnocercinae, a new subfamily of Dactylogyridae. American Midland Naturalist 52, 129–132.CrossRefGoogle Scholar
Moreira, J, Scholz, T, and Luque, JL (2015) First data on the parasites of Hoplias aimara (Characiformes): Description of two new species of gill monogeneans (Dactylogyridae). Acta Parasitologica 60(2), 254–260.CrossRefGoogle ScholarPubMed
Moreira, J, Luque, JL, and Šimková, A (2019) The phylogenetic position of Anacanthorus (Monogenea, Dactylogyridae) parasitizing Brazilian serrasalmids (Characiformes). Parasite 26, 44.CrossRefGoogle ScholarPubMed
Ñacari, LA, Sepulveda, FA, Escribano, R, and Oliva, ME (2017) Acanthocotyle gurgesiella n. sp. (Monogenea: Acanthocotylidae) from the deepsea skate Gurgesiella furvescens (Rajidae) in the south-eastern Pacific. Journal Helminthology 92, 223–227.CrossRefGoogle Scholar
Oliveira, C, Avelino, GS, Abe, KT, Mariguela, TC, Benine, RC, Ortí, G, Vari, RP, and Castro, RMC (2011) Phylogenetic relationships within the speciose family Characidae (Teleostei: Ostariophysi: Characiformes) based on multilocus analysis and extensive ingroup sampling. BMC Evolutionary Biology 11, 275.CrossRefGoogle ScholarPubMed
Oliveira, MSB, Santos-Neto, JF, Tavares-Dias, M, and Domingues, MV (2020) New species of Urocleidoides (Monogenoidea: Dactylogyridae) from the gills of two species of Anostomidae from the Brazilian Amazon, Brazilian. Journal Veterinary Parasitology 29(3), e007820.Google ScholarPubMed
Oliveira, GS, da Silva, RJ, Vieira, FEG, and Acosta, AA (2021) Urocleidoides spp. (Monogenea: Dactylogyridae) from the gills of Parodon nasus (Characiformes: Parodontidae) from a Brazilian stream with descriptions of two new species. Zootaxa 5081(4), 535–550.CrossRefGoogle ScholarPubMed
Plaisance, L, Rousset, V, Morand, S, and Littlewood, TDJ (2008) Colonization of Pacific islands by parasites of low dispersal ability: Phylogeography of two monogenean species parasitizing butterflyfishes in the South Pacific Ocean. Journal of Biogeography 35, 65–87.Google Scholar
Posada, D (2008) J ModelTest: Phylogenetic model averaging. Molecular Biology Evolution 25, 1253–1256.CrossRefGoogle Scholar
Price, CE and Bussing, WA (1968) Monogenean parasites of Costa Rican fishes. II. Proposal of Palombitrema heteroancistrium n. gen., n. sp. Proceedings of the Helminthological Society 35(1), 54–57.Google Scholar
Rambaut, A (2012) FigTree v1.4. Molecular evolution, phylogenetics and epidemiology. Available at http://tree.bio.ed.ac.uk/software/figtree/ (accessed 26 June 2020).Google Scholar
Rambaut, A, Suchard, MA, Xie, D, and Drummond, AJ (2014) Tracer v1.6. World Wide Web electronic publication. http://tree.bio.ed.ac.uk/software/tracer/.Google Scholar
Rasband, WS (2016) ImageJ. US National Institute of Health, Bethesda, Maryland, USA. Available at http://imagej.nih.gov/ij/ (accessed 02 January 2020).Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Rosim, DF, Mendoza-Franco, EF, and Luque, JL (2011) New and previously described species of Urocleidoides (Monogenoidea: Dactylogyridae) infecting the gills and nasal cavities of Hoplias malabaricus (Characiformes: Erythrinidae) from Brazil. Journal of Parasitology 97(3), 406–417.CrossRefGoogle ScholarPubMed
Rossin, MA and Timi, JT (2016) Dactylogyrid monogeneans parasitising Cyphocharax voga (Hensel) (Teleostei: Curimatidae) from the Pampas region, Argentina: New and previously described species. Systematic Parasitology 93, 701–714.CrossRefGoogle ScholarPubMed
Suriano, DM (1997) The genus Urocleidoides Mizelle and Price, 1964 (Monogenea: Ancyrocephalidae) parasitizing characoidei fishes in Argentina. Physis 53, 1–6.Google Scholar
Thompson, JD, Higgins, DG, and Gibson, TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Wu, XY, Zhu, XQ, Xie, MQ, and Li, AX (2006) The radiation of Haliotrema (Monogenea: Dactylogyridae: Ancyrocephalinae): Molecular evidence and explanation inferred from LSU rDNA sequences. Parasitology 132, 659–668.CrossRefGoogle ScholarPubMed
Yamada, FH, Brandão, H, POF, Yamada, and da Silva, RJ (2015) Philocorydoras longus n. sp. (Monogenea, Dactylogyridae) from the gills of Hoplosternum littorale (Siluriformes, Callichthyidae) in Southeastern Brazil and the reassignment of two species from the genus Urocleidoides to Philocorydoras. Helminthologia 52, 331–335.CrossRefGoogle Scholar
Zago, AC, Franceschini, L, Müller, MI, and da Silva, RJ (2018) A new species of Cacatuocotyle (Monogenea, Dactylogyridae) parasitizing Astyanax spp. (Characiformes, Characidae) from Brazil, including molecular data and a key to species identification. Acta Parasitological 63(2), 261–269.CrossRefGoogle Scholar
Zago, AC, Yamada, FH, Yamada, POF, Franceschini, L, Bongiovani, MF, and da Silva, RJ (2020) Seven new species of Urocleidoides (Monogenea: Dactylogyridae) from Brazilian fishes supported by morphological and molecular data. Parasitology Research 119(10), 3255–3283.CrossRefGoogle ScholarPubMed