Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T09:45:19.888Z Has data issue: false hasContentIssue false
  • English
  • Français

A new species of Loimopapillosum Hargis, 1955 (Monogenea: Monocotylidae) parasitizing Hypanus dipterurus (Myliobatiformes: Dasyatidae) off the Pacific coast of South America, and its phylogenetic relationships

Published online by Cambridge University Press:  21 July 2021

J.D. Chero Open the ORCID record for J.D. Chero [Opens in a new window] ,
C.L. Cruces Open the ORCID record for C.L. Cruces [Opens in a new window] ,
G. Sáez Open the ORCID record for G. Sáez [Opens in a new window] ,
A.G.L. Oliveira ,
C.P. Santos  and
J.L. Luque Open the ORCID record for J.L. Luque [Opens in a new window]
J.D. Chero
Affiliation:
Programa de Pós-Graduação em Biologia Animal da Universidade Federal Rural do Rio de Janeiro, BR 465, Km 7, CEP 23890-000, Seropédica, Rio de Janeiro, Brazil
C.L. Cruces
Affiliation:
Programa de Pós-Graduação em Biologia Animal da Universidade Federal Rural do Rio de Janeiro, BR 465, Km 7, CEP 23890-000, Seropédica, Rio de Janeiro, Brazil
G. Sáez
Affiliation:
Laboratorio de Parasitología General y Especializada, Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico Villarreal (UNFV), Código postal 15007, El Agustino, Lima, Peru
A.G.L. Oliveira
Affiliation:
Laboratório de Avaliação e Promoção da Saúde Ambiental, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil, 4365, Rio de Janeiro, RJ CEP 21040-360, Brazil
C.P. Santos
Affiliation:
Laboratório de Avaliação e Promoção da Saúde Ambiental, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil, 4365, Rio de Janeiro, RJ CEP 21040-360, Brazil
J.L. Luque*
Affiliation:
Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, CEP 23851-970, Seropédica, Rio de Janeiro, Brazil
*
Author for correspondence: J.L. Luque, E-mail: luqueufrrj@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

A new species of Loimopapillosum Hargis, 1955 is described based on specimens collected from the gills of the diamond stingray, Hypanus dipterurus (Jordan & Gilbert, 1880) (Myliobatiformes: Dasyatidae) captured off Puerto Pizarro, Tumbes Region, northern Peru. Loimopapillosum pascuali n. sp. is distinguished mainly from the type and only species, Loimopapillosum dasyatis Hargis, 1955, by its funnel-shaped male copulatory organ, with an asymmetrical base; the superficial root of the anchor with distal knobs; the deep root of the anchor with a constriction at its base; a single testis; and the number of head organs. Available sequences for members of Monocotylidae in the GenBank as well as partial sequences for the gene 28S and 18S ribosomal DNA from L. pascuali n. sp. were included in phylogenetic analyses, suggesting that Loimoinae (represented in this study by L. pascuali n. sp. and Loimosina sp.) is nested within the Monocotylidae Taschenberg, 1879. Therefore, we confirm the rejection of Loimoidae Price, 1936 and its reincorporation as a subfamily of Monocotylidae, as previously suggested. Loimopapillosum pascuali n. sp. represents the first species of this genus in South America.

Keywords

Elasmobranchdiamond stingrayLoimopapillosum pascuali n. spmarine fishes18s and 28s rDNAtaxonomy
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e37
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

Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Boeger, WA and Kritsky, DC (1993) Phylogeny and revised classification of the Monogenoidea Bychowsky, 1937 (Platyhelminthes). Systematic Parasitology 26, 1–32.CrossRefGoogle Scholar
Boeger, WA, Kritsky, DC, Domingues, MV and Bueno-Silva, M (2014) The phylogenetic position of the Loimoidae Price, 1936 (Monogenoidea: Monocotylidae) based on analyses of partial rDNA sequences. Parasitology International 63, 492–499.CrossRefGoogle ScholarPubMed
Bravo-Hollis, M (1969) Helmintos de peces del Pacífico Mexicano XXX. Descripción de tres monogéneos de la familia Monocotylidae Taschenberg, 1879. Anales del Instituto de Biología, Universidad Nacional Autónoma de México 40, 161–178.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Bychowsky, BE (1957) Monogenetic Trematodes, their classification and phylogeny. In Hargis, WH and A.I.B.S. (Eds) Izdatelstvo Academii Nauk, SSSR, Moscow and Leningrad (English translation). Washington, DC (in Russian).Google Scholar
Cao, S, Ding, X, Zhang, J and Liu, L (2010) Monogenea of Chinese marine fishes. XVIII. Two monocotylids, including a new species, from the blotched fantail ray Taeniurops meyeni (Elasmobranchii: Dasyatidae) in the South China Sea. Folia Parasitologica 57, 169–172.CrossRefGoogle Scholar
Chero, JD, Cruces, CL, Iannacone, I, Sáez, G, Sánchez, L, Minaya, D and Alvariño, L (2016) Monocotyle luquei n. sp. (Monogenea: Monocotylidae), from the gills of diamond stingray Dasyatis dipterura (Jordan and Gilbert, 1880) (Myliobatiformes: Dasyatidae), in the South Pacific. Acta Parasitologica 61, 713–719.CrossRefGoogle Scholar
Chero, JD, Cruces, CL, Sáez, G, Camargo, ACA, Santos, CP and Luque, JL (2018a) Hypanocotyle bullardi n. gen. n. sp. (Monogenea: Hexabothriidae) from gill of the diamond stingray Hypanus dipterurus (Jordan et Gilbert) (Myliobatiformes: Dasyatidae) in the Southeastern Pacific Ocean off Peru. Parasitology International 67, 425–430.CrossRefGoogle Scholar
Chero, JD, Cruces, CL, Sáez, G and Luque, JL (2018b) A new genus and species of the Dasybatotreminae Bychowsky, 1957 (Monogenea: Monocotylidae), parasitic on Hypanus dipterurus (Jordan & Gilbert) (Myliobatiformes: Dasyatidae) in the Southeastern Pacific Ocean off Peru. Zootaxa 4527, 347–356.CrossRefGoogle Scholar
Chero, JD, Cruces, CL, Sáez, G, Camargo, ACA, Santos, CP and Luque, JL (2019) Redescription and first nucleotide sequences of Rhinobatonchocotyle pacifica Oliva & Luque, 1995 (Monogenea: Hexabothriidae), a parasite of Pseudobatos planiceps (Garman, 1880) (Rhinopristiformes: Rhinobatidae) from Peru. Acta Parasitologica 64, 797–806.CrossRefGoogle ScholarPubMed
Chero, JD, Cruces, CL, Sáez, G, Santos, CP and Luque, JL (2020) A new species of Heterocotyle (Monogenea: Monocotylidae), a gill parasite of the diamond stingray Hypanus dipterurus (Myliobatiformes: Dasyatidae) from the Peruvian coastal zone. Acta Parasitologica 65, 474–481.CrossRefGoogle Scholar
Chisholm, LA (2013) Septesinus gibsoni n. g., n. sp. (Monocotylidae: Heterocotylinae), from the gills of Himantura walga (Dasyatidae) off Sarawak, Borneo. Systematic Parasitology 84, 255–264.CrossRefGoogle Scholar
Chisholm, LA and Kritsky, DC (2020) Heterocotyle whittingtoni n. sp. (Monogenea: Monocotylidae) from the gills of the black-spotted whipray, Maculabatis toshi (Whitley) (Myliobatiformes: Dasyatidae), collected in coastal waters of Queensland, Australia. Systematic Parasitology 97, 561–567.CrossRefGoogle Scholar
Chisholm, LA and Whittington, ID (2012) Three new species of Merizocotyle Cerfontaine, 1894 (Monogenea: Monocotylidae) from the nasal tissues of dasyatid rays collected off Malaysian and Indonesian Borneo. Systematic Parasitology 82, 167–176.CrossRefGoogle ScholarPubMed
Chisholm, LA, Wheeler, TA and Beverley-Burton, M (1995) A phylogenetic analysis and revised classification of the Monocotylidae Taschenberg, 1879 (Monogenea). Systematic Parasitology 32, 159–191.CrossRefGoogle Scholar
Chisholm, LA, Morgan, JAT, Adlard, RD and Whittington, ID (2001) Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. International Journal for Parasitology 31, 1253–1263.CrossRefGoogle ScholarPubMed
Doran, DJ (1953) New monogenetic trematodes from the shovelnose guitar fish, Rhinobatos productus (Ayres). Journal of Parasitology 39, 145–151.CrossRefGoogle Scholar
Dunn, KA, McEachran, JD and Honeycutt, RL (2003) Molecular phylogenetics of myliobatiform fishes (Chondrichthyes: Myliobatiformes), with comments on the effects of missing data on parsimony and likelihood. Molecular Phylogenetics and Evolution 27, 259–270.CrossRefGoogle Scholar
Eschmeyer, WN, Fricke, R and van der Laan, R (2019) Catalog of fishes: genera, species, references. Available at: http://www.calacademy.org (accessed 11 June 2020).Google Scholar
Hargis, WJ Jr (1955) Monogenetic trematodes of Gulf of Mexico fishes. Part V. The superfamily Capsaloidea. Transactions of the American Microscopical Society 74, 203–225.CrossRefGoogle Scholar
Humason, GL (1979) Animal tissue techniques. 4th edn. San Francisco, W. H: Freeman and Company, 661 pp.Google Scholar
Irigoitia, MM, Cantatore, DMP, Delpiani, GE, Incorvaia, IS, Lanfranchi, AL and Timi, JT (2014) Merizocotyle euzeti sp. n. (Monogenea: Monocotylidae) from the nasal tissue of three deep sea skates (Rajidae) in the southwestern Atlantic Ocean. Folia Parasitologica 61, 206–212.CrossRefGoogle Scholar
Irigoitia, MM, Chisholm, LA and Timi, JT (2016) A new species of Dendromonocotyle Hargis, 1955 (Monogenea: Monocotylidae) from the skin of Zearaja chilensis (Guichenot) (Rajiformes: Rajidae) from the Argentine Sea. Systematic Parasitology 93, 367–374.CrossRefGoogle ScholarPubMed
Irigoitia, MM, Braicovich, PE, Rossin, MA, Canel, D, Levy, E, Farber, MD and Timi, JT (2019) Diversity of Empruthotrema Johnston and Tiegs, 1992 parasitizing batoids (Chondrichthyes: Rajiformes and Myliobatiformes) from the Southwest Atlantic Ocean, with description of three new species. Parasitology Research 118, 3113–3127.CrossRefGoogle ScholarPubMed
Kitamura, K and Ogawa, K (2019) Three species of Dendromonocotyle Hargis, 1955 (Monogenea: Monocotylidae) collected from Japanese rays. Systematic Parasitology 96, 233–243.CrossRefGoogle ScholarPubMed
Kohn, A, Justo, MCN and Cohen, SC (2016) Monogenoidea. pp. 51–94 in Eiras, JC, Velloso, AL and Pereira, J Jr (Eds) Parasitos de peixes marinhos da América do Sul. Rio Grande, Editora FURG.Google Scholar
Kritsky, DC and Chisholm, LA (2020) Monocotylids (Monogenoidea) infecting elasmobranchs in Moreton Bay, Queensland, Australia, with descriptions of Calicotyle cutmorei n. sp. (Calicotylinae) and Dendromonocotyle raiae n. sp. (Monocotylinae). Systematic Parasitology 97, 569–589.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0. for bigger data. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle Scholar
Last, PR, Naylor, GJP and Manjaji-Matsumoto, BM (2016) A revised classification of the family Dasyatidae (Chondrichthyes: Myliobatiformes) based on new morphological and molecular insights. Zootaxa 4139, 345–368.CrossRefGoogle ScholarPubMed
Lebedev, BI (1988) Monogenea in the light of new evidence and their position among platyhelminths. Angewandte Parasitologie 29, 149–167.Google ScholarPubMed
Lopes, DA, Mainenti, A, Sanches, M, Knoff, M and Gomes, DC (2016) Type material of Platyhelminthes (Monogenoidea) housed in the Helminthological Collection of the Oswaldo Cruz Institute/ FIOCRUZ (CHIOC), Rio de Janeiro, Brazil, from 1979 to 2016. Zookeys 616, 1–75.Google Scholar
Luque, JL, Cruces, C, Chero, J, Paschoal, F, Alves, PV, Da Silva, AC, Sánchez, L and Iannacone, J (2016) Checklist of metazoan parasites of fishes from Peru. Neotropical Helminthology 10, 301–375.Google Scholar
Mendoza-Garfias, B, García-Prieto, L and Pérez-Ponce de León, G (2017) Checklist of the Monogenea (Platyhelminthes) parasitic in Mexican aquatic vertebrates. Zoosystema 39, 501–598.CrossRefGoogle Scholar
Merlo-Serna, AI and García-Prieto, L (2016) A checklist of helminth parasites of Elasmobranchii in Mexico. Zookeys 563, 73–128.Google Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2011) The CIPRES science gateway: a community resource for phylogenetic analyses. pp.1–8 in Proceedings of the 2011 TeraGrid Conference: Extreme Digital Discovery, Salt Lake City, Utah, July 18 - 21, 2011.CrossRefGoogle Scholar
Ñacari, LA, Sepulveda, FA, Escribano, R and Oliva, ME (2018) Acanthocotyle gurgesiella n. sp. (Monogenea: Acanthocotylidae) from the deep-sea skate Gurgesiella furvescens (Rajidae) in the south-eastern Pacific. Journal of Helminthology 92, 223–227.CrossRefGoogle Scholar
Ñacari, LA, Sepulveda, FA, Escribano, R and Oliva, ME (2019) Two new species of Acanthocotyle Monticelli, 1888 (Monogenea: Acanthocotylidae), parasites of two deep-sea skates (Elasmobranchii: Rajiformes) in the South-East Pacific. Parasites & Vectors 12, 512.CrossRefGoogle ScholarPubMed
Ñacari, LA, Sepulveda, FA, Droguet, F, Escribano, R and Oliva, ME (2020) Calicotyle hydrolagi n. sp. (Monogenea: Monocotylidae) infecting the deep-sea Eastern Pacific black ghost shark Hydrolagus melanophasma from the Atacama Trench, with comments on host specificity of Calicotyle spp. Parasitology International 75, 102025.CrossRefGoogle Scholar
Neifar, L, Euzet, L and Ben Hassine, OK (2002) Une nouvelle espèce de Monocotylidae (Monogenea) parasite branchial de Rinobatos cemiculus (Euselachii, Rhinobatidae), avec proposition d'un nouveau genre et d'un amendement à la diagnose des Monocotylidae. Zoosystema 24, 699–706.Google Scholar
Nelson, JS (2006) Fishes of the world. 4th edn. Hoboken, New Jersey, USA, John Wiley & Sons, Inc., 624.Google Scholar
Pollerspöck, J and Straube, N (2021) Bibliography database of living/fossil sharks, rays and chimaeras (Chondrichthyes: Elasmobranchii, Holocephali): host-parasite list and parasite-host list. Available at: http://www.shark-references.com (accessed 17 January 2021).Google Scholar
Posada, D and Crandall, KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics (Oxford, England) 14, 817–818.CrossRefGoogle ScholarPubMed
Ronquist, F, Huelsenbeck, J and Teslenko, M (2011) Draft MrBayes version 3.2 manual: tutorials and model summaries. Distributed with the software from http://brahms.biology.rochester.edu/software.html.Google Scholar
Santos, CP, Santos, AL, Cunha, R and Chisholm, LA (2012) A new species of Heterocotyle Scott, 1904 (Monogenea: Monocotylidae) from the gills of Dasyatis guttata (Dasyatidae) in southwestern Atlantic waters off Rio de Janeiro, Brazil. Systematic Parasitology 81, 65–70.CrossRefGoogle ScholarPubMed
Sinnappah, ND, Lim, LHS, Rohde, K, Tinsley, R, Combes, C and Verneau, O (2001) A paedomorphic parasite associated with a neotenic amphibian host: phylogenetic evidence suggests a revised systematic position for Sphyranuridae within anuran and turtle polystomatoineans. Molecular Phylogenetics and Evolution 18, 189–201.CrossRefGoogle ScholarPubMed
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
Vaughan, D and Chisholm, L (2010) Heterocotyle tokoloshei sp. nov. (Monogenea, Monocotylidae) from the gills of Dasyatis brevicaudata (Dasyatidae) kept in captivity at Two Oceans Aquarium, Cape Town, South Africa: description and notes on treatment. Acta Parasitologica 55, 108–114.CrossRefGoogle Scholar