Folia Parasitologica, vol. 63 (2016)

Folia Parasitologica 63:020 (2016) | DOI: 10.14411/fp.2016.020

The life cycle of Huffmanela huffmani Moravec, 1987(Nematoda: Trichosomoididae), an endemic marine-relict parasite of Centrarchidae from a Central Texas spring

McLean L. D. Worsham1, David G. Huffman1, František Moravec2, J. Randy Gibson3
1 Freeman Aquatic Biology, Texas State University, San Marcos, TX, USA;
2 Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic;
3 U.S. Fish and Wildlife Service, Aquatic Resources Center, San Marcos, TX, USA

The life cycle of the swim bladder nematode Huffmanela huffmani Moravec, 1987 (Trichinelloidea: Trichosomoididae), an endemic parasite of centrarchid fishes in the upper spring run of the San Marcos River in Hays County, Texas, USA, was experimentally completed. The amphipods Hyalella cf. azteca (Saussure), Hyalella sp. and Gammarus sp. were successfully infected with larvated eggs of Huffmanela huffmani. After ingestion of eggs of H. huffmani by experimental amphipods, the first-stage larvae hatch from their eggshells and penetrate through the digestive tract to the hemocoel of the amphipod. Within about 5 days in the hemocoel of the experimental amphipods at 22 °C, the larvae presumably attained the second larval stage and were infective for the experimental centrarchid definitive hosts, Lepomis spp. The minimum incubation period before adult nematodes began laying eggs in the swim bladders of the definitive hosts was found to be about 7.5 months at 22 °C. This is the first experimentally completed life cycle within the Huffmanelinae.

Keywords: swim bladder nematode, Trichinelloidea, development, intermediate host, Amphipoda, Hyalella, Gammarus, fish, USA

Received: January 12, 2016; Accepted: April 14, 2016; Published online: June 10, 2016


References

  1. Anderson R.C. 2000: Nematode Parasites of Vertebrates: Their Development and Transmission. CABI Publishing, Wallingford, 650 pp.
  2. Anderson R.C., Chabaud A.G. Willmott S. 2009: Keys to the Nematode Parasites of Vertebrates: Archival Volume. CABI Publishing, Wallingford, 463 pp.
  3. van Banning P. 1980: The occurrence of black spots in the tongue sole, Cynoglossus browni Chabanaud, due to nematode eggs (Capillaria spinosa) previously described in the shark Carcharhinus milberti Muller & Henle. J. Fish Biol. 17: 305-309. Go to original source...
  4. Bowles D.E., Arsuffi T.L. 1993: Karst aquatic ecosystems of the Edwards Plateau region of central Texas, USA: a consideration of their importance, threats to their existence, and efforts for their conservation. Aquat. Conserv. 3: 317-329. Go to original source...
  5. Bullard S.A., Ruiz C.F., McElwain A., Murray M.J., Borucinska J.D. Benz G.W. 2012: Huffmanela cf. carcharhini (Nematoda: Trichosomoididae: Huffmanelinae) from skin of a sandbar shark, Carcharhinus plumbeus, in the Pacific Ocean. J. Parasitol. 98: 333-340. Go to original source... Go to PubMed...
  6. Carballo M.C., Navone G.T. Cremonte F. 2011: Parasites of the silversides Odontesthes smitti and Odontesthes nigricans (Pisces: Atherinopsidae) from Argentinean Patagonia. Comp. Parasitol. 78: 95-103. Go to original source...
  7. Casazza T.L., Ross S.W. 2008: Fishes associated with pelagic Sargassum and open water lacking Sargassum in the Gulf Stream off North Carolina. Fish. Bull. 106: 348-363.
  8. Cox M.K. 1998: The distribution and life cycle of Huffmanela huffmani (Nematoda: Trichosomoididae). MSc. thesis, Southwest Texas State University, San Marcos, 54 pp.
  9. Cox M.K., Huffman D.G. Moravec F. 2004: Observations on the distribution and biology of Huffmanela huffmani (Nematoda: Trichosomoididae). Folia Parasitol. 51: 50-54. Go to original source... Go to PubMed...
  10. Cross J.H. 1992: Intestinal capillariasis. Clin. Microbiol. Rev. 5: 120-129. Go to original source... Go to PubMed...
  11. Diaz P.H., Alexander M.L. 2010: Aquatic macroinvertebrates of a spring-fed ecosystem in Hays County, Texas, USA. Ent. News. 121: 478-486. Go to original source...
  12. Edwards S.W., Arnold C.R. 1961: The caddis flies of the San Marcos River. Tex. J. Sci. 13: 398-415.
  13. Esteves A., Seixas F., Carvalho S., Nazário N., Mendes M. Martins C. 2009: Huffmanela sp. (Nematoda: Trichosomoididae) muscular parasite from Trisopterus luscus captured off the Portuguese coast. Dis. Aquat. Organ. 84: 251-255. Go to original source... Go to PubMed...
  14. Gibson J.R., Harden S.J., Fries J.N. 2008: Survey and distribution of invertebrates from selected springs of the Edwards Aquifer in Comal and Hays Counties, Texas. Southwest. Nat. 53: 74-84. Go to original source... Go to PubMed...
  15. Groeger A.W., Brown P.F., Tietjen T.E. Kelsey T.C. 1997: Water quality of the San Marcos River. Tex. J. Sci. 49: 279-294.
  16. Hasslinger M.A., Schwarzler C. 1980: Blasenwurm der Ratte, Trichosomoides crassicauda: Untersuchungen zu Entwicklung, Ubertragung und Diagnose. Berl. Munch. Tierarztl. Wochenschr. 93: 132-135. Go to PubMed...
  17. Holsinger J.R., Longley G. 1980: The Subterranean Amphipod Crustacean Funa of an Artesian Well in Texas. Smithsonian Institution Press, Washington D.C., 62 pp.
  18. Huffman D.G., Moravec F. 1988: First description of adult Huffmanela huffmani Moravec, 1987 (Nematoda: Trichosomoididae) from the swim bladder of centrarchid fishes of the upper San Marcos River, central Texas. Folia Parasitol. 35: 227-234. Go to PubMed...
  19. Janicki K., Rašín K. 1930: Bemerkungen über Cystoopsis acipenseri des Wolga-Sterlets, sowie über die Entwicklung dieses Nematoden in Zwischenwirt. Z. Wissenschaft. Zool. 136: 1-37.
  20. Justine J.L. 2004: Three new species of Huffmanela Moravec, 1987 (Nematoda: Trichosomoididae) from the gills of marine fish off New Caledonia. Syst. Parasitol. 59: 29-37. Go to original source... Go to PubMed...
  21. Justine J.L. 2005: Huffmanela lata n. sp. (Nematoda: Trichosomoididae: Huffmanelinae) from the shark Carcharhinus amblyrhynchos (Elasmobranchii: Carcharhinidae) off New Caledonia. Syst. Parasitol. 61: 181-184. Go to original source... Go to PubMed...
  22. Justine J.L. 2007: Huffmanela spp. (Nematoda, Trichosomoididae) parasites in coral reef fishes off New Caledonia, with descriptions of H. balista n. sp. and H. longa n. sp. Zootaxa 1628: 23-41.
  23. Justine J.L. 2011: Huffmanela plectropomi n. sp. (Nematoda: Trichosomoididae: Huffmanelinae) from the coral grouper Plectropomus leopardus (Lacépède) off New Caledonia. Syst. Parasitol. 79: 139-143. Go to original source... Go to PubMed...
  24. Justine J.L., Iwaki T. 2014: Huffmanela hamo sp. n. (Nematoda: Trichosomoididae: Huffmanelinae) from the dagger-tooth pike conger Muraenesox cinereus off Japan. Folia Parasitol. 61: 267-271. Go to original source... Go to PubMed...
  25. Kasparsone Z.V. 1984: [New data on the development of the nematode Capillaria corvorum (Rudolphi, 1819) Travassos, 1915 in the organism of Corvus frigilegus L.]. Izv. AN Latv. SSR. 8: 115-117. (In Russian.)
  26. Køie M., Nylund A. 2001: The life-cycle of Capillaria gracilis (Capillariidae), a nematode parasite of gadoid fish. Sarsia 86: 383-387. Go to original source...
  27. Kutzer E., Otte E. 1966: Capillaria petruschewskii (Schulman, 1948): Morphologie, Biologie und pathogene Bedeutung. Z. Parasitenkd. 28: 16-30. Go to original source... Go to PubMed...
  28. Löwenstein S. 1910: Epithelwucherungen und Papillombildungen der Rattenblase, verursacht durch ein Trichosoma (Tr. crassicauda?). Beitr. Klin. Chirurg. 69: 533-546.
  29. MacLean R.A., Fatzinger M.H., Woolard K.D. Harms C.A. 2006: Clearance of a dermal Huffmanela sp. in a sandbar shark (Carcharhinus plumbeus) using levamisole. Dis. Aquat. Organ. 73: 83. Go to original source... Go to PubMed...
  30. Markevich A.P. 1951: Parasitic Fauna of Freshwater Fish of the Ukrainian SSR. Publ. House of the USSR Acad. Sci., Kiev, 376 pp.
  31. Michel G.D. 1984: The Biology of Capillaria sp. (Nematoda: Capillariidae) from Swim Bladders of Sunfishes of the Upper San Marcos River. MS thesis, Southwest Texas State University, San Marcos, 59 pp.
  32. Moravec F. 1987: Revision of Capillariid Nematodes (subfamily Capillariinae) Parasitic in Fishes. Studie ČSAV No. 3. Academia, Praha, 144 pp.
  33. Moravec F. 2001: Trichinelloid Nematodes Parasitic in Cold-Blooded Vertebrates. Academia, Praha, 432 pp.
  34. Moravec F., Campbell B.G. 1991: A new Huffmanela species, H. schouteni sp. n. (Nematoda: Trichosomoididae) from flying fishes in Curaçao. Folia Parasitol. 38: 29-32. Go to PubMed...
  35. Moravec F., Conboy G.A. Speare D.J. 2005: A new trichosomoidid from the skin of Sebastes spp. (Pisces) from British Columbia, Canada. J. Parasitol. 91: 411-414. Go to original source... Go to PubMed...
  36. Moravec F., Fajer-Avila E. 2000: Huffmanela mexicana n. sp. (Nematoda: Trichosomoididae) from the marine fish Sphoeroides annulatus in Mexico. J. Parasitol. 86: 1229-1231. Go to original source... Go to PubMed...
  37. Moravec F., Garibaldi F. 2000: Huffmanela paronai sp. n. (Nematoda: Trichosomoididae), a new parasite from the skin of swordfish Xiphias gladius in the Ligurian Sea (Western Mediterranean). Folia Parasitol. 47: 309-314. Go to original source... Go to PubMed...
  38. Moravec F., Garibaldi F. 2003: First record of Huffmanela schouteni (Nematoda: Trichosomoididae), a histozoic parasite of flying-fishes, in Europe. Dis. of Aquat. Organ. 57: 173-175. Go to original source... Go to PubMed...
  39. Moravec F., Koudela B., Ogawa K. Nagasawa K. 1998: Two new Huffmanela species, H. japonica n. sp. and H. shikokuensis n. sp. (Nematoda: Trichosomoididae), from marine fishes in Japan. J. Parasitol. 84: 589-593. Go to original source... Go to PubMed...
  40. Moravec F., Prokopič J., Shlikas A.V. 1987: The biology of nematodes of the family Capillariidae Neveu-Lemaire, 1936. Folia Parasitol. 34: 39-56. Go to PubMed...
  41. Morehouse N.F. 1942: Life cycle of Capillaria caudinflata, a nematode parasite of the common fowl. Iowa State College, Ames, Iowa, 133 pp.
  42. Near T.J., Bolnick D.I., Wainwright P.C. 2005: Fossil calibrations and molecular divergence time estimates in centrarchid fishes (Teleostei: Centrarchidae). Evolution. 59: 1768-1782. Go to original source... Go to PubMed...
  43. O'Docharty E.M. 2007: Studies on the Life Cycle of Huffmanela huffmani (Nematoda: Trichosomoididae). MS thesis, Texas State University, San Marcos, Texas, 55 pp.
  44. Othman M.S., Pascoe D. 2001: Growth, development and reproduction of Hyalella azteca (Saussure, 1858) in laboratory culture. Crustaceana 74: 171-181. Go to original source...
  45. Palko B.J., Beardsley G.L., Richards W.J. 1981: Synopsis of the biology of the swordfish, Xiphias gladius Linnaeus. NOAA Tech. Rep. NMFS Circ., 441 pp.
  46. Raupach M.J., Barco A., Steinke D., Beermann J., Laakmann S., Mohrbeck I., Neumann H., Kihara T.C., Pointner K. Radulovici A. 2015: The application of DNA barcodes for the identification of marine crustaceans from the North Sea and adjacent regions. PLoS ONE 10: e0139421. Go to original source... Go to PubMed...
  47. Romashov B.V. 1980: Life cycle of Capillaria erinacei (Nematoda, Capillariidae). Helminthologia 17: 181-189.
  48. Ruiz C.F., Bullard S.A. 2013: Huffmanela markgracei sp. n. (Nematoda: Trichosomoididae) from buccal cavity of Atlantic sharpnose shark, Rhizoprionodon terraenovae (Carcharhiniformes: Carcharhinidae), in the northwestern Gulf of Mexico off Texas. Folia Parasitol. 60: 353-358. Go to original source... Go to PubMed...
  49. Ruiz C.F., Ray C.L., Cook M., Grace M.A. Bullard S.A. 2013: A new species of Trichosomoididae (Nematoda) from skin of red snapper (Perciformes: Lutjanidae), on the Texas-Louisiana Shelf, Northern Gulf of Mexico. J. Parasitol. 99: 318-326.
  50. Serejo C.S. 2004: Cladistic revision of talitroidean amphipods (Crustacea, Gammaridea), with a proposal of a new classification. Zool. Scr. 33: 551-586. Go to original source...
  51. Shlikas A.V. 1967: [Ontogenesis of the nematodes Capillaria bursata Freitas et Almeida, 1934 and Capillaria caudinflata (Molin, 1858) Travassos, 1915]. Acta Parasitol. Lithuan. 7: 119-130. (In Russian.)
  52. Shlikas A.V. 1978: [Studies on the development of the nematode Trichocephalus leporis Froelich, 1789 in the organism of the definitive host.]. Acta Parasitol. Lithuan. 16: 81-87. (In Russian.)
  53. Thomas L.J. 1924: Studies on the life history of Trichosomoides crassicauda (Bellingham). J. Parasitol. 10: 105-136. Go to original source...
  54. TISI 2015: Redbreast Sunfish (Lepomis auritus). Texas Invasive Species Institute, Huntsville, Texas.
  55. Underwood H.T., Dronen N.O. 1984: Endohelminths of fishes from the upper San Marcos River, Texas. Southwest. Nat. 29: 377-385. Go to original source...
  56. Wahl D.V., Chapman W.H. 1967: The application of data on the survival of eggs of Trichosomoides crassicauda (Bellingham) to the control of this bladder parasite in laboratory rat colonies. Lab. Anim. Care 17: 386-390. Go to PubMed...