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Type: Article
Published: 2019-07-18
Page range: 507–533
Abstract views: 77
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Occurrence of Podocotyle Dujardin, 1845 (Opecoelidae, Podocotylinae) in three species of deep-sea macrourids from the Gulf of Mexico and Caribbean Sea with an updated key to species and host-parasite checklist

Corpus Christi Museum of Science & History, 1900 N. Chaparral St., Corpus Christi, Texas 78401, U.S.A.
Laboratory of Parasitology, Department of Wildlife & Fisheries Sciences, Wildlife, Fisheries & Ecological Sciences Building, TAMU
Laboratory of Parasitology, Department of Wildlife & Fisheries Sciences, Wildlife, Fisheries & Ecological Sciences Building, TAMU 2258, Bldg. 1537, 534 John Kimbrough Blvd., College Station, Texas 77843, U.S.A.
Acanthocephala Bathygadus favosus Bathygadus melanobranchus Caribbean Sea Colombia Deep sea Digenea Florida Gadiformes Gulf of Mexico Macrouridae Mexico Nezumia atlantica Opecoelidae Podocotylinae Podocotyle pearsei Podocotyle sp. 1 Podocotyle sp. 2 Podocotyle sp. 3

Abstract

Podocotyle pearsei Manter, 1934 is documented from the intestine of Vaillant’s grenadier, Bathygadus melanobranchus Vaillant (Macrouridae: Bathygadinae), collected from the northeastern and western Gulf of Mexico from 783–841 m depth. The finding of P. pearsei in B. melanobranchus represents the first originally published report of this genus from this host and the fifth documented host species for P. pearsei. We report three unidentified species of Podocotyle, represented by one individual each, from the intestine of the western Atlantic grenadier, Nezumia atlantica (Parr) (Macrouridae: Macrourinae), and from Bathygadus favosus Goode & Bean (Macrouridae: Bathygadinae) found at 637 m, 710 m and 1,143 m depths in the northeastern Gulf of Mexico off Florida and from the Caribbean Sea off Colombia. We provide a checklist of the parasites known from the three macrourid species relevant to this study, comment on the biogeography of the five species of Podocotyle now known from the deep sea and discuss the low host specificity observed across this genus. The high number of fish hosts for Podocotyle (i.e. type hosts include at least 22 piscine families) encompassing a wide phylogenetic diversity and diet makes it unlikely that members of a single genus could evolve such a broad array of life histories (i.e. utilize dissimilar intermediate hosts), and we predict in the future that Podocotyle will be taxonomically divided up. Morphological and especially molecular work is needed for Podocotyle as well as for other digenean genera known to inhabit the deep sea. Podocotyle sp. 1 & 2 represent the first originally published reports of this genus from N. atlantica while Podocotyle sp. 3 represents the first report of this genus from B. favosus. Podocotyle koshari Nagaty, 1973 is declared a species inquirenda, and a dichotomous key to the 27 species of Podocotyle we recognize is provided.

 

References

  1. Acena, S.P. (1941) Preliminary notes on a trematode with two yolk reservoirs and a new species of Lecithochirium. The Philippine Journal of Science, 75, 285–289.

    Armstrong, H.W. (1974) A study of the helminth parasites of the family Macrouridae from the Gulf of Mexico and Caribbean Sea: their systematics, ecology and zoogeographical implications. PhD dissertation, Texas A&M University, College Station, Texas, 329 pp.

    Bartoli, P. & Gibson, D.I. (1991) On Podocotyle scorpaenae, Poracanthium furcatum and Derogenes latus, three poorly known digenean parasites of western Mediterranean teleosts. Systematic Parasitology, 20, 29–46.

    https://doi.org/10.1007/BF00009709

    Bartoli, P. & Gibson, D.I. (2007) Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the western Mediterranean. Journal of Natural History, 41, 1553–1570.

    https://doi.org/10.1080/00222930701500142

    Bartoli, P. & Jousson, O. (2003) The life-cycle of Podocotyle scorpaenae (Opecoelidae: Digenea) demonstrated by comparative analysis of ribosomal DNA sequences. In: Combes, C. & Jourdane, J. (Eds.), Taxonomy, ecology and evolution of metazoan parasites. (Livre hommage á Louis Euzet). Vol. 1. Presses Universitaires de Perpignan, Perpignan Cedex, pp. 17–28.

    Bartoli, P., Bray, R.A. & Gibson, D.I. (2003) Opecoelidae (Digenea) from western Mediterranean fishes: three rare species. Systematic Parasitology, 55, 81–95.

    https://doi.org/10.1023/A:1024097231987

    Blend, C.K. (1996) The digenetic trematodes parasitizing macrourid fishes from the Gulf of Mexico and Caribbean Sea: an examination of their systematics, zoogeography and host-parasite ecology. M.S. thesis, Texas A&M University, College Station, Texas, 305 pp.

    Blend, C.K. & Dronen, N.O. (2015) Description of a new species of Podocotyle Dujardin, 1845 (Digenea: Opecoelidae: Plagioporinae) from the cusk-eel, Luciobrotula corethromycter Cohen, 1964 (Ophidiiformes: Ophidiidae), from the Gulf of Mexico and Caribbean Sea. Acta Parasitologica, 60, 234–243.

    https://doi.org/10.1515/ap-2015-0033

    Blend, C.K., Dronen, N.O. & Armstrong, H.W. (2004) Macrourimegatrema brayi n. gen., n. sp. (Digenea: Opecoelidae) from four species of deep-sea macrourid fishes from the Gulf of Mexico and Caribbean Sea, with a list of endohelminths reported from species of Bathygadus and Gadomus (Macrouridae). Zootaxa, 566 (1), 1–18.

    https://doi.org/10.11646/zootaxa.566.1.1

    Blend, C.K., Dronen, N.O. & Armstrong, H.W. (2016) Podocotyle nimoyi n. sp. (Digenea: Opecoelidae: Plagioporinae) and a re-description of Podocotyle pearsei Manter, 1934 from five species of deep-sea macrourids from the Gulf of Mexico and Caribbean Sea. Zootaxa, 4117 (4), 491–512.

    https://doi.org/10.11646/zootaxa.4117.4.3

    Blend, C.K., Dronen, N.O., Racz, G.R. & Gardner, S.L. (2017) Pseudopecoelus mccauleyi n. sp. and Podocotyle sp. (Digenea: Opecoelidae) from the deep waters off Oregon and British Columbia with an updated key to the species of Pseudopecoelus von Wicklen, 1946 and checklist of parasites from Lycodes cortezianus (Perciformes: Zoarcidae). Acta

    Parasitologica, 62, 231–254.

    https://doi.org/10.1515/ap-2017-0031

    Bray, R.A. (1995) Annotated checklist of digenean parasites of Macrouridae (Teleostei, Gadiformes). Acta Parasitologica, 40, 168–192.

    Bray, R.A. & Campbell, R.A. (1996) New plagioporines (Digenea: Opecoelidae) from deep-sea fishes of the North Atlantic Ocean. Systematic Parasitology, 33, 101–113.

    https://doi.org/10.1007/BF00009426

    Bray, R.A., Littlewood, D.T.J., Herniou, E.A., Williams, B. & Henderson, R.E. (1999) Digenean parasites of deep-sea teleosts: a review and case studies of intrageneric phylogenies. Parasitology, 119 (Supplement), S125–S144.

    https://doi.org/10.1017/S0031182000084687

    Brinkmann, A. Jr. (1975) Trematodes of Greenland. Meddelelser om Grønland, 205, 1–88.

    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, 575–583.

    https://doi.org/10.2307/3284227

    Ching, H.L. (1960) Some digenetic trematodes of fishes of Friday Harbor, Washington. Journal of Parasitology, 46, 241–250.

    https://doi.org/10.2307/3275181

    Ching, H.L. (1979) The life cycle of Podocotyle enophrysi Park, 1937 (Trematoda: Opecoelidae). Canadian Journal of Zoology, 57, 1341–1344.

    https://doi.org/10.1139/z79-172

    Cohen, D.M., Inada, T., Iwamoto, T. & Scialabba, N. (1990) Gadiform Fishes of the World (Order Gadiformes). An Annotated and Illustrated Catalogue of Cods, Hakes, Grenadiers and Other Gadiform Fishes Known to Date. FAO Fisheries Synopsis. No. 125. Vol. 10. FAO, Rome, 442 pp.

    Creplin, F.Ch.H. (1825) Observationes de Entozois. I. Gryphiswaldiae, Mauritii Librarii, 86 pp.

    https://doi.org/10.5962/bhl.title.10158

    Cribb, T.H. (2005) Family Opecoelidae Ozaki, 1925. In: Jones, A., Bray, R.A. & Gibson, D.I. (Eds.), Keys to the Trematoda. Vol. 2. CABI Publishing and the Natural History Museum, Wallingford, pp. 443–531.

    Dollfus, R.-Ph. (1968) Les trématodes de l’histoire naturelle des helminthes de Félix Dujardin (1845). Mémoires du Muséum National d’Histoire Naturelle, Series A, 54, 118–196.

    Dujardin, F. (1845) Histoire Naturelle des Helminthes ou vers Intestinaux. Librarie Encylopedie de Roret, Paris, 654 + 15 pp.

    https://doi.org/10.5962/bhl.title.10123

    Fischthal, J.H. & Thomas, J.D. (1970) Digenetic trematodes of marine fishes from Ghana: Family Opecoelidae. Proceedings of the Helminthological Society of Washington, 37, 129–141.

    Froese, R. & Pauly, D. (Eds.) (2019) FishBase. World Wide Web electronic publication. Version 02/2019. Available from: http://www.fishbase.org (accessed 26 March 2019)

    Gibson, D.I. (1976) Monogenea and Digenea from fishes. Discovery Reports, 36, 179–266.

    Gibson, D.I. (1986) Podocotyle araii sp. nov. (Digenea: Opecoelidae) from Sebastes spp. off the coast of British Columbia, with a key to the species of Podocotyle Dujardin, 1845, occurring off the Pacific coast of North America. Journal of Natural History, 20, 735–743.

    https://doi.org/10.1080/00222938600770511

    Gibson, D.I. & Bray, R.A. (1982) A study and reorganization of Plagioporus Stafford, 1904 (Digenea: Opecoelidae) and related genera, with special reference to forms from European Atlantic waters. Journal of Natural History, 16, 529–559.

    https://doi.org/10.1080/00222938200770431

    Gibson, D.I. & Bray, R.A. (1984) On Anomalotrema Zhukov, 1957, Pellamyzon Montgomery, 1957, and Opecoelina Manter, 1934 (Digenea: Opecoelidae), with a description of Anomalotrema koiae sp. nov. from North Atlantic waters. Journal of Natural History, 18, 949–964.

    https://doi.org/10.1080/00222938400770831

    Hunninen, A.V. & Cable, R.M. (1943) The life history of Podocotyle atomon (Rudolphi) (Trematoda: Opecoelidae). Transactions of the American Microscopical Society, 62, 57–68.

    Issaitschikow, I.M. (1928) Zur Kenntnis der parasitischen Würmer einiger Gruppen von Wirbeltieren der russischen Arktis. Trudy Morskogo Nauchnogo Instituta, Moskva, 3, 5–79.

    Jensen, K. (2009) Cestoda (Platyhelminthes) of the Gulf of Mexico. In: Felder, D.L. & Camp, D.K. (Eds.), Gulf of Mexico Origin, Waters and Biota. Vol. 1. Biodiversity. Texas A&M University Press, College Station, pp. 487–522.

    Johnson, W.F. (1949) A new species of trematode, Podocotyle gibbonsia, from tide pool fishes of Monterey Bay, California. Transactions of the American Microscopical Society, 68, 107–109.

    https://doi.org/10.2307/3223258

    Jousson, O., Bartoli, P. & Pawlowski, J. (1999) Molecular identification of developmental stages in Opecoelidae (Digenea). International Journal for Parasitology, 29, 1853–1858.

    https://doi.org/10.1016/S0020-7519(99)00124-1

    Klimpel, S., Seehagen, A., Palm, H.-W. & Rosenthal, H. (2001) Deepwater metazoan fish parasites of the world. Logos Verlag, Berlin, 315 pp.

    Klimpel, S., Busch, M.W., Kellermanns, E., Kleinertz, S. & Palm, H.-W. (2009) Metazoan deep-sea fish parasites. Verlag Natur & Wissenschaft, Solingen, 384 pp.

    Køie, M. (1981) On the morphology and life-history of Podocotyle reflexa (Creplin, 1825) Odhner, 1905, and a comparison of its developmental stages with those of P. atomon (Rudolphi, 1802) Odhner, 1905 (Trematoda: Opecoelidae). Ophelia, 20, 17–43.

    https://doi.org/10.1080/00785236.1981.10426560

    Linton, E. (1910) Helminth fauna of the Dry Tortugas. II. Trematodes. Papers from the Tortugas Laboratory of the Carnegie Institute of Washington, 4, 11–98.

    Linton, E. (1940) Trematodes from fishes mainly from the Woods Hole region, Massachusetts. Proceedings of the United States National Museum, 88, 1–172.

    https://doi.org/10.5479/si.00963801.88-3078.1

    Lloyd, L.C. (1938) Some digenetic trematodes from Puget Sound fish. Journal of Parasitology, 24, 103–133.

    https://doi.org/10.2307/3272491

    Lühe, M.F.L. (1900) Ueber die Gattung Podocotyle (Duj.) Stoss. Zoologisches Anzeiger, 23, 487–492.

    MacKenzie, K. & Gibson, D.I. (1970) Ecological studies of some parasites of plaice Pleuronectes platessa L. and flounder Platichthys flesus (L.). Symposia of the British Society for Parasitology, 8, 1–42.

    Maillard, C. & Lambert, M. (1978) Plagioporus novellus n. sp. (Trematoda, Opecoelidae), parasite de Conger conger (Téléostei). Annales de Parasitologie, Paris, 53, 367–371.

    Manter, H.W. (1926) Some North American fish trematodes. Illinois Biological Monographs, 10, 127–264.

    https://doi.org/10.5962/bhl.title.50240

    Manter, H.W. (1934) Some digenetic trematodes from deep-water fish of Tortugas, Florida. Papers from Tortugas Laboratory, 28, 257–345.

    Manter, H.W. (1940) Digenetic trematodes of fishes from the Galapagos Islands and the neighboring Pacific. Allan Hancock Pacific Expeditions, 2, 325–497.

    Manter, H.W. (1947) The digenetic trematodes of marine fishes of Tortugas, Florida. The American Midland Naturalist, 38, 257–416.

    https://doi.org/10.2307/2421571

    Manter, H.W. (1954a) Some digenetic trematodes from fishes of New Zealand. Transactions of the Royal Society of New Zealand, 82, 475–568.

    Manter, H.W. (1954b) Trematoda of the Gulf of Mexico. Fishery Bulletin of the Fish and Wildlife Service, 55, 335–350.

    Martin, S.B., Cutmore, S.C., Ward, S. & Cribb, T.H. (2017) An updated concept and revised composition for Hamacreadium Linton, 1920 (Opecoelidae: Plagioporinae) clarifies a previously obscured pattern of host-specificity among species. Zootaxa, 4254 (2), 151–187.

    https://doi.org/10.11646/zootaxa.4254.2.1

    Martin, S.B., Huston, D.C., Cutmore, S.C. & Cribb, T.H. (2018) A new classification for deep-sea opecoelid trematodes based on the phylogenetic position of some unusual taxa from shallow-water, herbivorous fishes off south-west Australia. Zoological Journal of the Linnean Society, 20, 1–29.

    McEachran, J.D. & Fechhelm, J.D. (1998) Fishes of the Gulf of Mexico. Vol 1. Myxiniformes to Gasterosteiformes. University of Texas Press, Austin, 1112 pp.

    Miller, M.J. (1941) A critical study of Stafford’s report on “Trematodes of Canadian Fishes” based on his trematode collection. Canadian Journal of Research, Series D, 19, 28–52.

    https://doi.org/10.1139/cjr41d-003

    Moser, M. & Noble, E.R. (1977) Zschokkella (Protozoa: Myxosporida) in macrourid fishes. International Journal for Parasitology, 7, 97–100.

    https://doi.org/10.1016/0020-7519(77)90073-x

    Moser, M., Noble, E.R. & Lee, R.S. (1976) The genus Myxidium (Protozoa: Myxosporida) in macrourid fishes. Journal of Parasitology, 62, 685–689.

    https://doi.org/10.2307/3278938

    Nagaty, H.F. (1941) Trematodes of fishes from the Red Sea. Part 2. The genus Hamacreadium Linton, 1910 (Fam. Allocreadiidae) with a description of two new species. The Journal of the Egyptian Medical Association, 24, 300–310.

    Nagaty, H.F. (1973) Trematodes of fishes from the Red Sea. Parts 1 to 20. a recapitulation. Bulletin of the Society of Zoology of Egypt, 25, 1–13.

    Nagaty, H.F. & Abdel Aal, T.M. (1962) Trematodes of fishes from the Red Sea. Part 19. On three new species of Podocotyle (Family Allocreadiidae). Journal of Parasitology, 48, 746–747.

    https://doi.org/10.2307/3275268

    Nicoll, W. (1913) New trematode parasites from fishes of the English Channel. Parasitology, 5, 238–246.

    https://doi.org/10.1017/S0031182000000366

    Nicoll, W. (1914) The trematode parasites of fishes from the English Channel. Journal of the Marine Biological Association of the United Kingdom, 10, 466–505.

    https://doi.org/10.1017/S0025315400008250

    Odhner, T. (1905) Trematoden des arktischen Gebietes. Fauna Arctica, 4, 289–372.

    Overstreet, R.M., Cook, J.O. & Heard, R.W. (2009) Trematoda (Platyhelminthes) of the Gulf of Mexico. In: Felder, D.L. & Camp, D.K. (Eds.), Gulf of Mexico origin, waters and biota.Vol. 1. Biodiversity. Texas A&M University Press, College Station, pp. 419–486.

    Park, J.T. (1937) A revision of the genus Podocotyle (Allocreadiinae), with a description of eight new species from tide pool fishes from Dillon’s Beach, California. Journal of Parasitology, 23, 405–422.

    https://doi.org/10.2307/3272235

    Parona, C. (1899) Catalogo di eminti raccolti in vertebrati dell’Isola d’Elba dal dott, Giacomo Damiani. Bolletino dei Musei de Zoologia e Anatomia Comparata della Reale Universitá di Genova, 77, 1–16.

    Pritchard, M.H. (1966) A revision of the genus Podocotyle (Trematoda Opecoelidae). Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 93, 158–172.

    Rudolphi, C.A. (1802) Fortsetzung der Beobachtungen uber die Eingeweidewurmer. Archiv für Zoologie und Zootomie, 2, 1– 67.

    Rudolphi, C.A. (1819) Entozoorum synopsis, cui accedunt mantissa duplex et indices locupletissimi. Rucker, Berolini, 811 pp.

    https://doi.org/10.5962/bhl.title.9157

    Shen, J. & Qiu, Z. (1995) Studies on the Trematodes of Fishes from the Yellow Sea and the Bo Hai Sea, Science Press, Beijing, 207 pp.

    Shimazu, T. (1990) Trematodes of a new genus, Neoplagioporus gen. n. (Digenea: Opecoelidae: Plagioporinae), and an unidentified opecoelid from freshwater fishes of Japan. Japanese Journal of Parasitology, 39, 384–396.

    Skrjabin, K.I. & Koval, V.P. (1958) Coitocaecinae Poche, 1925; Plagioporinae Manter, 1947. In: Skjrabin, K.I. (Ed.), Trematodes of Animals and Man, 15, pp. 329–818.

    Sokolov, S.G., Shchenkov, S.V. & Gordeev, I.I. (2018) Records of opecoeline species Pseudopecoelus cf. vulgaris and Anomalotrema koiae Gibson & Bray, 1984 (Trematoda, Opecoelidae, Opecoelinae) from fish of the North Pacific, with notes on the phylogeny of the family Opecoelidae. Journal of Helminthology, 93 (4), 475–485.

    https://doi.org/10.1017/S0022149X18000573

    Stafford, J. (1904) Trematodes from Canadian fishes. Zoologischer Anzeiger, 27, 481–495.

    Stiles, C.W. & Hassall, A. (1898) An inventory of the genera and subgenera of the trematode family Fasciolidae. Archives de Parasitologie, Paris, 1, 81–99.

    Stossich, M. (1892) Osservazioni elmintologiche. Glasnik Hrvatskoga Narodoslovnoga Drustva, Zagreb, 7, 64–73.

    Szidat, L. (1944) Weitere Untersuchungen über die Trematodenfauna einheimischer Süsswasserfische. II. Mitteilung die Gattung Sphaerostoma (Stiles & Hassall 1898) Looss 1899 und Verwandte. Zeitschrift fur Parasitenkunde, 13, 183–214.

    https://doi.org/10.1007/BF02122205

    Takahashi, S. (1928) On a new trematode Podocotyle ayu n. sp. from the intestine of Plecoglossus altivelis (T. and S.). Acta Medica Okayama, 1, 51–56.

    Wang, Y.-Y., Wang, P.-Q. & Zhang, W.-H. (1992) Opecoelid trematodes of marine fishes from Fujian Province. Wuyi Science Journal, 9, 67–89.

    WoRMS Editorial Board (2019) Podocotyle Dujardin, 1845. Accessed through: World Register of Marine Species (WoRMS) Available from: http://www.marinespecies.org/aphia.php?p=taxdetails&id=108540 (accessed 26 March 2019)

    Yamaguti, S. (1958) Systema Helminthum. Vol. 1. The digenetic trematodes of vertebrates. Part 1. Interscience Publishers, New York, 979 pp.

    Yamaguti S. (1970) Digenetic Trematodes of Hawaiian Fishes. Keigaku Publishing Company, Tokyo, 436 pp..

    Yamaguti, S. (1971) Synopsis of digenetic trematodes of vertebrates. Vol. 1. Keigaku Publishing Company, Tokyo, 1074 pp.