Abstract
Heteropriapulus Kritsky, 2007 (Monogenea: Dactylogyridae), which originally included only two species from the gills of loricariid catfishes, is reviewed and six newly described species from loricariids in the Paraná River basin in Brazil are added. Diagnosis of the genus is amended and a key to the species identification is provided. Heteropriapulus anchoradiatus n. sp. from Pterygoplichthys ambrosettii (Holmberg) (Hypostominae) differs from its congeners by having a long sclerotized vagina, ventral anchors with short shaft and conspicuous superficial root, and a conspicuous and robust postero-medial process on the dorsal bar; H. bitomus n. sp. from the same fish host differs by the presence of two pairs of sclerotized patches associated with the ventral anchors; H. falxus n. sp. from Hypostomus strigaticeps (Regan) (Hypostominae) and Hypostomus ancistroides (Ihering) (Hypostominae) is unique by the shape of the accessory piece composed of two strongly sclerotized subunits; H. microcleithrus n. sp. from P. ambrosettii differs by presenting the smallest length of the dorsal bar and unique shape of the longer subunit of the accessory piece resembling the ‘hammer and sickle’ shape; H. pterygoplichthyi n. sp. from the same host presents unique shape of the longer subunit of the accessory piece of the cirrus, which is represented by ‘two sickles’ jointed by the base; and H. semitortus n. sp. from Rhinelepis aspera Spix & Agassiz (Rhinelepinae) can be distinguished by the accessory piece composed of a single straight unit and a cirrus tube with the highest number of spiral rings at the proximal end (2½). First molecular data for this genus (partial sequences of the 28S rRNA gene) are provided including the type species H. heterotylus (Jogunoori, Kritsky & Venkatanarasaiah, 2004).
References
Armbruster, J.W. (2011) Global Catfish Biodiversity. American Fisheries Society Symposium, 77, 15–37.
Azevedo, R.K., Abdallah, V.D. & Luque, J.L. (2010) Acanthocephala, Annelida, Arthropoda, Myxozoa, Nematoda and Platyhelminthes parasites of fishes from the Guandu River, Rio de Janeiro, Brazil. Check List, 6, 659–667.
https://doi.org/10.15560/6.4.659Behrmann-Godel, J., Roch, S. & Brinker, A. (2013) Gill worm Ancyrocephalus percae (Ergens, 1966) outbreak negatively impacts the Eurasian perch Perca fluviatus L. stock of Lake Constance, Germany. Journal of Fish Diseases, 37, 925–930.
https://doi.org/10.1111/jfd.12178
Boeger, W.A. & Belmont-Jégu, E. (1994) Neotropical Monogenoidea. 21. Trinigyrus mourei sp. n. (Dactylogyridae) from the gills of the Amazonian catfish Hypostomus marginatus (Loricariidae). Amazoniana, 13, 13–16.
Braga, M.P., Araújo, S.B.L. & Boeger, W.A. (2014) Patterns of interaction between Neotropical freshwater fishes and their gill Monogenoidea (Platyhelminthes). Parasitology Research, 113, 481–490.
https://doi.org/10.1007/s00436-013-3677-8
Branches, B. & Domingues, M.V. (2014) A new species of Unilatus (Platyhelminthes: Monogenoidea) from the gills of Leporacanthicus galaxias Isbrücker et Nijssen (Siluriformes: Loricariidae) from Brazil. Acta Parasitologica, 59, 91–97.
https://doi.org/10.2478/s11686-014-0213-7
Burguess, W.E. (1989) An Atlas of Freshwater and Marine Catfishes—A Preliminary Survey of the Siluriformes. T.F.H. Publications, Inc., Neptune City, NJ, 784 pp.
Chisholm, L.A., Morgan, J.A.T., Adlard, R.D. & Whittington, I.D. (2001) Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. International Journal for Parasitology, 31, 1537–1547.
https://doi.org/10.1016/S0020-7519(01)00313-7
Cohen, S.C. & Kohn, A. (2008) New data on species of Demidospermus (Dactylogyridae: Monogenea) parasitizing fishes from the reservoir of the Itaipu Hydroelectric Power Station, Paraná State, Brazil, with new synonymies. Revista Brasileira de Parasitologia Veterinária, 17, 167–170.
https://doi.org/10.1590/S1984-29612008000300011
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristice and parallel computing. Nature Methods, 9, 772.
https://doi.org/10.1038/nmeth.2109
Ergens, R. (1969). The suitability of ammonium picrate-glycerin in preparing slides of lower Monogenoidea. Folia Parasitologica, 16, 320.
Eschmeyer, W.N. & Fong, J.D. (2017) Species by family/subfamily. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp (accessed 10 April 2017)
Euzet, L. & Combes, C. (1980) Les problèmes de l’espèce chez les animaux parasites. In: Les problèmes de l’espèce dans le règne animal. Mémoire n° 40 de la Société Zoologique de France, 3, pp. 239–285.
Ferrari-Hoeinghaus, A.P., Bellay, S., Takemoto, R.M. & Pavanelli, G.C. (2010) A new species of Demidospermus Suriano, 1983 (Monogenea, Dactylogyridae) parasitic on Loricariichthys platymetopon Isbrücker et Nijssen (Loricariidae, Siluriformes) from the Upper Paraná River floodplain, Brazil. Acta Parasitologica, 55, 16–19.
https://doi.org/10.2478/s11686-010-0007-5
Franceschini, L., Zago, A.C., Müller, M.I., Francisco, C.J., Takemoto, R.M. & Silva, R.J. (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. [published online]
https://doi.org/10.1017/S0022149X17000256
Froese, R. & Pauly, D. (2016) FishBase. World Wide Web electronic publication. Version 11/2014. Available from: http://www.fishbase.org/search.php (accessed 29 April 2016)
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/10.1080/10635150390235520Gonçalves, R.A., Oliveira, M.S.B., Santos, E.F. & Tavares-Dias, M. (2014) Aspectos ecológicos da comunidade de parasitos em duas espécies de Loricariidae da bacia Igarapé Fortaleza, estado do Amapá, Brasil. Biota Amazônia, 4, 15–21.
https://doi.org/10.18561/2179-5746/biotaamazonia.v4n1p15-21
Gusev, A.V. (1985) Key to parasites of the freshwater fish fauna of the USSR. Vol 2. Nauka, Leningrad, 424 pp. [Bauer, O.N. (Ed.), in Russian]
Hanek, G., Molnar, K. & Fernando, C.H. (1974) Three new genera of Dactylogyridae (Monogenea) from freshwater fishes of Trinidad. Journal of Parasitology, 60, 911–913.
https://doi.org/10.2307/3278510Humason, G.L. (1979) Animal tissue techniques. W.H. Freeman Co., San Francisco, California, 661 pp.
Jogunoori, W., Kritsky, D.C. & Venkatanarasaiah, 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 (Polyochoinea: Dactylogyridae). Systematic Parasitology, 58, 115–124.
https://doi.org/10.1023/B:SYPA.0000029422.16712.9a
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. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.
https://doi.org/10.1093/bioinformatics/bts199
Kritsky, D.C. (2007) Heteropriapulus nom. nov. (Monogenoidea: Dactylogyridae) for Heterotylus Jogunoori, Kritsky and Venkatanarasaiah, 2004, a junior homonym of Heterotylus Kirsch in Reitter, 1913 (Coleoptera: Curculionidae). Systematic Parasitology, 68, 223.
http://dx.doi.org./10.1007/s11230-007-9111-9
Kritsky, D.C., Boeger, W.A. & Thatcher, V.E. (1985) Neotropical Monogenea. 7. Parasites of pirarucu, Arapaima gigas (Cuvier), with descriptions of two new species and redescription of Dawestrema cycloancistrium Price and Nowlin, 1967 (Dactylogyridae: Ancyrocephalinae). Proceedings of the Biological Society of Washington, 98, 321–331.
Kritsky, D.C., Boeger, W.A. & Thatcher, V.E. (1986a) Neotropical Monogenea. 9. Status of Trinigyrus Hanek, Molnar & Fernando, 1974 (Dactylogyridae) with descriptions of two new species from loricariid catfishes from the Brazilian Amazon. Proceedings of the Biological Society of Washington, 99, 392–398.
Kritsky, D.C. & Mizelle, J.D. (1968) Studies on monogenetic trematodes. XXXV. Some new and previously described North American species of Gyrodactylus. American Midland Naturalist, 79, 205–215.
https://doi.org/10.2307/2423166Kritsky, D.C., Thatcher, V.E. & Boeger, W.A. (1986b) Neotropical Monogenea. 8. Revision of Urocleidoides (Dactylogyridae, Ancyrocephalinae). Proceedings of the Helminthological Society of Washington, 53, 1–37.
Li, H. & Huang, Q. (2012) One new Chinese record genera (Ancyrocephalidae) and one new species and one new recorded of Monogenea parasiting on gills of Hypostomus plecostomus. Journal of Dalian Ocean University, 27, 116–119. [in Chinese]
Littlewood, D.T.J., Curini-Galletti, M. & Herniou, E.A. (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution, 16, 449–466.
http://dx.doi.org./10.1006/mpev.2000.0802
Lockyer, A.E., Olson, P.D. & Littlewood, D.T.J. (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society, 78, 155–171.
https://doi.org/10.1046/j.1095-8312.2003.00141.x
Mendoza-Franco, E.F., Mendoza-Palmero, C.A. & 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, 847–862.
https://doi.org/10.1007/s11230-016-9671-7
Mendoza-Palmero, C.A., Blasco-Costa, I. & Scholz, T. (2015) Molecular phylogeny of Neotropical monogeneans (Platyhelminthes: Monogenea) from catfishes (Siluriformes). Parasites and Vectors, 8, 164.
https://doi.org/10.1186/s13071-015-0767-8
Mendoza-Palmero, C.A., Scholz, T., Mendoza-Franco, E.F. & Kuchta, R. (2012) New species and geographical records of dactylogyrids (Monogenea) of catfish (Siluriformes) from the Peruvian Amazonia. Journal of Parasitology, 98, 484–497.
https://doi.org/10.1645/GE-2941.1
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, LA, pp. 1–8.
Mizelle, J.D. (1936) New species of trematodes from the gills of Illinois fishes. American Midland Naturalist, 17, 785–806.
https://doi.org/10.2307/2420687Mizelle, J.D. & Klucka, A.R. (1953) Studies on monogenetic trematodes. XIV. Dactylogyridae from Wisconsin fishes. American Midland Naturalist, 49, 720–733.
https://doi.org/10.2307/2485203Mizelle, J.D. & Kritsky, D.C. (1967a) Unilatus gen. n., a unique Neotropical genus of Monogenea. Journal of Parasitology, 53, 1113–1114.
https://doi.org/10.2307/3276854Mizelle, J.D. & Kritsky, D.C. (1967b) Studies on monogenetic trematodes. XXX. Five new species of Gyrodactylus from the Pacific tomcod, Microgadus proximus (Girard). Journal of Parasitology, 53, 263–269.
https://doi.org/10.2307/3276572Mizelle, J.D., Kritsky, D.C. & Crane, J.W. (1968) Studies on monogenetic trematodes XXXVIII. Ancyrocephalinae from South America with the proposal of Jainus gen. n. American Midland Naturalist, 80, 186–198.
https://doi.org/10.2307/2423609Molnar, K., Hanek, G. & Fernando, C.H. (1974) Ancyrocephalids (Monogenea) from freshwater fishes of Trinidad. Journal of Parasitology, 60, 914–920.
https://doi.org/10.2307/3278511Nelson, J.S. (2006) Fishes of the world. 4th Edition. John Wiley & Sons, New York, 601 pp.
Nitta, M. & Nagasawa, K. (2013) First Japanese record of Heteropriapulus heterotylus (Monogenea: Dactylogyridae), from the alien catfish Pterygoplichthys disjunctivus (Siluriformes: Loricariidae) in Okinawa. Species Diversity, 18, 281–284.
https://doi.org/10.12782/sd.18.2.281
Olson, P.D., Cribb, T.H., Tkach, V.V., Bray, R.A. & Littlewood, D.T.J. (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755.
https://doi.org/10.1016/S0020-7519(03)00049-3
Pleijel, F., Jondelius, U., Norlinder, E., Nygren, A., Oxelman, B., Schander, C., Sundberg, P. & Thollesson, M. (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution, 48, 369–371.
https://doi.org/10.1016/j.ympev.2008.03.024
Price, C.H.E. (1968) Diaccessorius, a new genus of Monogenea from the gills of an Amazon River teleost. Acta Biologica Venezuelica, 6, 84–89.
Rambaut, A. (2009) FigTree version 1.3.1 [computer program]. Available from: http://tree.bio.ed.ac.uk (accessed 14 June 2017)
Řehulková, E., Mendlová, M. & Šimková, A. (2013) Two new species of Cichlidogyrus (Monogenea: Dactylogyridae) parasitizing the gills of African cichlid fishes (Perciformes) from Senegal: morphometric and molecular characterization. Parasitology Research, 112, 1399–1410.
https://doi.org/10.1007/s00436-013-3291-9
Reis, R.E., Weber, C. & Malabarba, L.R. (1990) Review of the genus Hypostomus Lacépède, 1803 from southern Brazil, with descriptions of three new species (Pisces, Siluriformes, Loricariidae). Revue Suisse de Zoologie, 97, 729–766.
Reitter, E. (1913) Bestimmungs-Schlüssel der mir bekannten europäischen Gattungen de Curculionidae, mit Einschluss de mir bekannten Gattungen aus dem palaearctischen Gebiete. Verhandlungen des naturforschenden Vereines in Brünn, 51, 1–90.
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
https://doi.org/10.1093/sysbio/sys029Rodríguez-Santiago, M.A., García-Prieto, L., Mendoza-Garfias, B., González-Solís, D. & Grano-Maldonado, M.I. (2016) Parasites of two coexisting invasive sailfin catfishes (Siluriformes: Loricariidae) in a tropical region of Mexico. Neotropical Ichthyology, 14 (3), e160021.
https://doi.org/10.1590/1982-0224-20160021
Rodríguez-Santiago, M.A., Grano-Maldonado, M., Ávila, E. & Gómez, S. (2015) Occurrence of Heteropriapulus heterotylus (Monogenoidea: Dactylogyridae), ectoparasite of two invasive sailfin catfishes (Siluriformes: Loricariidae) from the southeastern Mexico. Neotropical Helminthology, 9, 55–64.
Sela, I., Ashkenazy, H., Katoh, K., Pupko, T. (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Research, 43, W7–W14.
https://doi.org/10.1093/nar/gkv318Šimková, A., Matějusová, I. & Cunningham, C.O. (2006) A molecular phylogeny of the Dactylogyridae sensu Kritsky & Boeger (1989) based on the D1–D3 domains of large subunit rDNA. Parasitology, 133, 43–53.
https://doi.org/10.1017/S0031182006009942Stamatakis, A. (2014) RaxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1013.
https://doi.org/10.1093/bioinformatics/btu033Suriano, D.M. (1983) Demidospermus anus gen. nov. sp. nov. (Monogenea: Ancyrocephalinae) parasite branquial de Loricaria (L.) anus Valenciennes, 1840 (Pisces: Loricariidae) de la Laguna de Chascomus - Provincia de Buenos Aires - Republica Argentina. Neotropica, 29, 111–119.
Suriano, D.M. (1985) El genero Unilatus Mizelle y Kritsky, 1967 (Monogenea: Ancyrocephalidae) del Rio Negro, Manaus, Brasil. Neotropica, 31, 163–175.
Thatcher, V.E. (2006) Amazon Fish Parasites. 2nd Edition. Pensoft, Sofia, 508 pp.
Werle, E.C., 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.
https://doi.org/10.1093/nar/22.20.4354Wu, X.Y., Zhu, X.Q., Xie, M.Q. & Li, A.X. (2006) The radiation of Haliotrema (Monogenea: Dactylogyridae: Ancyrocephalinae): molecular evidence and explanation inferred from LSU rDNA sequences. Parasitology, 132, 659–68.
https://doi.org/10.1017/S003118200500956X
Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26, 1–7.
https://doi.org/10.1016/S1055-7903(02)00326-3Zawadzki, C.H., Weber, C., Pavanelli, C.S. & Renesto, E. (2002) Morphological and biochemical comparison of two allopatric populations of Hypostomus margaritifer (Regan, 1907) (Osteichthyes, Loricariidae) from the upper Paraná River basin, Brazil. Acta Scientiarum Biological Science, 24, 499–505.
Zica, E.O.P., Abdallah, V.D, Azevedo, R.K., Wunderlich, A.C., Carvalho, E.D. & Silva, R.J. (2012) Unilatus unilatus Mizelle & Kritsky, 1967 (Monogenea, Ancyrocephalinae) in Hypostomus spp. (Siluriformes, Loricariidae) from the Chavantes reservoir, São Paulo State, Brazil. Helminthologia, 49, 87–91.
https://doi.org/10.2478/s11687-012-0018-x