Folia Parasitologica, vol. 63 (2016)

Folia Parasitologica 63:008 (2016) | DOI: 10.14411/fp.2016.008

A synoptic review of Promonobothrium Mackiewicz, 1968 (Cestoda: Caryophyllidea), parasites of suckers (Catostomidae) in North America, with description of two new species

Mikuláš Oros1,2, Jan Brabec2, Roman Kuchta2, Anindo Choudhury3, Tomáš Scholz2
1 Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovak Republic;
2 Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, and Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic;
3 Division of Natural Sciences, St. Norbert College, DePere, Wisconsin, USA

Monozoic cestodes of the recently amended genus Promonobothrium Mackiewicz, 1968 (Cestoda: Caryophyllidea), parasites of suckers (Cypriniformes: Catostomidae) in North America, are reviewed, with information on their host specificity, distribution and data on the scolex morphology of seven species studied for the first time using scanning electron microscopy (SEM). Evaluation of type and voucher specimens from museum collections and newly collected material of most species indicated the following valid nominal species: Promonobothrium minytremi Mackiewicz, 1968 (type species); P. ingens (Hunter, 1927); P. hunteri (Mackiewicz, 1963); P. ulmeri (Calentine et Mackiewicz, 1966); P. fossae (Williams, 1974) and P. mackiewiczi (Williams, 1974). Rogersus Williams, 1980 with its only species R. rogersi is transferred to Promonobothrium based on morphological and molecular data. Promonobothrium currani sp. n. and P. papiliovarium sp. n. are described from Ictiobus bubalus (Rafinesque) and Ictiobus niger (Rafinesque), and Erimyzon oblongus (Mitchill), respectively. The newly described species can be distinguished from the other congeners by the morphology of the scolex, the position of the anteriormost vitelline follicles and testes, the presence of postovarian vitelline follicles and the shape of the ovary. Molecular phylogenetic analyses of six species based on sequences of the small and large subunits of the nuclear ribosomal RNA genes (ssrDNA, lsrDNA) confirmed the monophyletic status of the genus and supported the validity of the species analysed. A key to identification of all species of Promonobothrium based on morphological characteristics is provided.

Keywords: Eucestoda, fish, comparative morphology, taxonomy, new species, Nearctic Region, identification key, molecular phylogeny

Received: November 30, 2015; Accepted: February 15, 2016; Published online: March 23, 2016


References

  1. Bangham R.V., Venard C.E. 1942: Studies on parasites of Reelfoot lake fish. IV. Distribution on studies and checklist of parasites. J. Tennessee Acad. Sci. 17: 22-38.
  2. Barčák D., Oros M., Hanzelová V., Scholz T. 2014: Phenotypic plasticity in Caryophyllaeus brachycollis Janiszewska, 1953 (Cestoda: Caryophyllidea): does fish host play a role? Syst. Parasitol. 88: 153-166. Go to original source... Go to PubMed...
  3. Bazsalovicsová E., Kráľová-Hromadová I., Brabec J., Hanzelová V., Oros M., Scholz T. 2014: Conflict between morphology and molecular data: a case of the genus Caryophyllaeus (Cestoda, Caryophyllidea), monozoic tapeworm of cyprinid fishes. Folia Parasitol. 61: 346-352. Go to original source...
  4. Brabec J., Scholz T., Kráľová-Hromadová I., Bazsalovicsová E., Olson P.D. 2012: Substitution saturation and nuclear paralogs of commonly employed phylogenetic markers in the Caryophyllidea, an unusual group of non-segmented tapeworms (Platyhelminthes). Int. J. Parasitol. 42: 259-267. Go to original source... Go to PubMed...
  5. Caira J.N., Jensen K., Barbeau E. 2012: Global Cestode Database. World Wide Web electronic publication, www.tapewormdb.uconn.edu, 12/2015.
  6. Calentine R.L. 1967: Larval development of four caryophyllaeid cestodes. Proc. Iowa Acad. Sci. 72: 418-424.
  7. Calentine R.L., Mackiewicz J.S. 1966: Monobothrium ulmeri n. sp. (Cestoda: Caryophyllaeidae) from North American Catostomidae. Trans. Am. Microsc. Soc. 85: 516-520. Go to original source...
  8. Chen W.-J., Mayden R.L. 2012: Phylogeny of suckers (Teleostei: Cypriniformes: Catostomidae): further evidence of relationships provided by the single-copy nuclear gene IRBP2. Zootaxa 3586: 195-210.
  9. Chervy L. 2009: Unified terminology for cestode microtriches: a proposal from the International Workshops on Cestode Systematics in 2002-2008. Folia Parasitol. 56: 199-230. Go to original source... Go to PubMed...
  10. Dayrat B. 2005: Towards integrative taxonomy. Biol. J. Linnean Soc. 85: 407-415. Go to original source... Go to PubMed...
  11. Doosey M.H., Bart H.L., Saitoh K., Miya M. 2010: Phylogenetic relationships of catostomid fishes (Actinopterygii: Cypriniformes) based on mitochondrial ND4/ND5 gene sequences. Mol. Phyl. Evol. 54: 1028-1034. Go to original source... Go to PubMed...
  12. Grimes L.R., Miller G.C. 1975: Caryophyllaeid cestodes in the creek chubsucker, Erimyzon oblongus (Mitchill), in North Carolina. J. Parasitol. 61: 973-974. Go to original source... Go to PubMed...
  13. Haley D.R., Barger M.A. 2014: A new genus and species of caryophyllaeid (Cestoda: Caryophyllidea) from spotted suckers, Minytrema melanops (Catostomidae), in the Big Thicket national preserve, Texas, U.S.A. Comp. Parasitol. 81: 23-26. Go to original source... Go to PubMed...
  14. Hanzelová V., Oros M., Barčák D., Miklisová D., Kirin D., Scholz T. 2015: Morphological polymorphism in tapeworms: redescription of Caryophyllaeus laticeps (Pallas, 1781) (Cestoda: Caryophyllidea) and characterisation of its morphotypes from different fish hosts. Syst. Parasitol. 90: 177-190. Go to original source... Go to PubMed...
  15. Hoffman G.L. 1999: Parasites of North American freshwater fishes. Second Edition. Comstock Publishing Associates, Cornell University Press, Ithaca, New York, 539 pp.
  16. Hunter G.W. 1927: Notes on the Caryophyllaeidae of North America. J. Parasitol. 14: 16-26. Go to original source...
  17. Hunter G.W. 1930: Studies on the Caryophyllaeidae of North America. Illin. Biol. Monogr. 11 (1927), 186 pp. Go to PubMed...
  18. Jenkins R.E., Burkhead N.M. 1993: Freshwater Fishes of Virginia. American Fisheries Society. Bethesda, Maryland, 1 079 pp.
  19. Katoh K., Standley D.M. 2013: MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30: 772-780. Go to original source... Go to PubMed...
  20. 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. Go to original source... Go to PubMed...
  21. Králová-Hromadová I., Štefka J., Špakulová M., Orosová M., Bombarová M., Hanzelová V., Bazsalovicsová E., Scholz T. 2010: Intra-individual internal transcribed spacer 1 (ITS1) and ITS2 ribosomal sequence variation linked with multiple rDNA loci: a case of triploid Atractolytocestus huronensis, the monozoic cestode of common carp. Int. J. Parasitol. 40: 175-181. Go to original source... Go to PubMed...
  22. Lanfear R., Calcott B., Ho S.Y.W., Guindon S. 2012: Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29: 1695-1701. Go to original source... Go to PubMed...
  23. Mackiewicz J.S. 1963: Monobothrium hunteri sp. n. (Cestoidea: Caryophyllaeidae) from Catostomus commersoni (Lacépède) (Pisces: Catostomidae) in North America. J. Parasitol. 49: 723-730. Go to original source...
  24. Mackiewicz J.S. 1968: Two new caryophyllaeid cestodes from the spotted sucker, Minytrema melanops (Raf.) (Catostomidae). J. Parasitol. 54: 808-813. Go to original source...
  25. Mackiewicz J.S. 1972: Caryophyllidea (Cestoidea): a review. Exp. Parasitol. 31: 417-512. Go to original source... Go to PubMed...
  26. Mackiewicz J.S. 1981: Caryophyllidea (Cestoidea): evolution and classification. Adv. Parasitol. 19: 139-206. Go to original source... Go to PubMed...
  27. Mackiewicz J.S. 1994: Order Caryophyllidea van Beneden in Carus, 1863. In: L.F. Khalil, A. Jones and R.A. Bray (Eds.), Keys to the Cestode Parasites of Vertebrates. CAB International, Wallingford, pp. 21-43.
  28. Mackiewicz J.S. 2003: Caryophyllidea (Cestoidea): molecules, morphology and evolution. Acta Parasitol. 48: 143-154.
  29. Nelson J.S. 2006: Fishes of the World. John Wiley and Sons, New York, 624 pp.
  30. Oros M., Scholz T., Hanzelová V., Mackiewicz J.S. 2010: Scolex morphology of monozoic cestodes (Caryophyllidea) from the Palaearctic Region: a useful tool for species identification. Folia Parasitol. 57: 37-46. Go to original source... Go to PubMed...
  31. Page L.M., Burr B.M. 1991: A Field Guide to Freshwater Fishes of North America North of Mexico. Houghton Mifflin Company, Massachusetts, 432 pp.
  32. 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. Mol. Phylogen. Evol. 48: 369-371. Go to original source... Go to PubMed...
  33. 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. Syst. Biol. 61: 539-542. Go to original source... Go to PubMed...
  34. Schaeffner B.C., Jirků M., Mahmoud Z.N., Scholz T. 2011: Revision of Wenyonia (Cestoda: Caryophyllidea) from Synodontis catfish in Africa. Syst. Parasitol. 79: 83-107. Go to original source... Go to PubMed...
  35. Schlick-Steiner B.C. Steiner F.M., Seifert B., Stauffer C., Christian E., Crozier R.H. 2010: Integrative taxonomy: a multisource approach to exploring biodiversity. Annu. Rev. Entomol. 55: 421-438. Go to original source... Go to PubMed...
  36. Schmidt G.D. 1986: CRC Handbook of Tapeworm Identification. CRC Press, Boca Raton, Florida, 675 pp.
  37. Scholz T., Brabec J., Kráľová-Hromadová I., Oros M., Bazsalovicsová E., Ermolenko A., Hanzelová V. 2011: Revision of Khawia spp. (Cestoda: Caryophyllidea), parasites of cyprinid fish, including a key to their identification and molecular phylogeny. Folia Parasitol. 58: 197-223. Go to original source... Go to PubMed...
  38. Scholz T., Choudhury A. 2014: Parasites of freshwater fishes in North America: why so neglected? J. Parasitol. 100: 26-45. Go to original source... Go to PubMed...
  39. Scholz T., Oros M., Choudhury A., Brabec J., Waeschenbach A. 2015: New circumscription of freshwater fish parasites Monobothrium Diesing, 1863 and Promonobothrium Mackiewicz, 1968 (Cestoda: Caryophyllidea) using morphological and molecular evidence. J. Parasitol. 101: 29-36. Go to original source... Go to PubMed...
  40. Špakulová M., Orosová M., Mackiewicz J.S. 2011: Cytogenetics and chromosomes of tapeworms (Platyhelminthes, Cestoda). Adv. Parasitol. 74: 177-230. Go to original source... Go to PubMed...
  41. Sun Y.H., Xie C.X., Wang W.M., Liu S.Y., Treer T., Chang M.M. 2007: The genetic variation and biogeography of catostomid fishes based on mitochondrial and nucleic DNA sequences. J. Fish Biol. 70: 291-309. Go to original source...
  42. Williams D.D. 1977: Biacetabulum oregoni sp. n. (Cestoda: Caryophyllidea) from Catostomus macrocheilus. Iowa State J. Res. 52: 397-400.
  43. Williams D.D. 1978: A key to caryophyllaeid cestodes of Wisconsin fishes. Iowa State J. Res. 51: 471-477.
  44. Williams E.H. 1974: Two new species of Monobothrium (Cestoda: Caryophyllaeidae) from catostomid fishes of the southeastern United States. Trans. Am. Fish. Soc. 103: 610-615. Go to original source...
  45. Williams E.H. 1980: Rogersus rogersi gen. et sp. n. (Cestoda: Caryophyllaeidae) from the blacktail redhorse, Moxostoma poecilurum (Jordan) (Osteichthyes), in the soustheastern United States. J. Parasitol. 66: 564-568. Go to original source...
  46. Zwickl D.J. 2006: Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis, University of Texas at Austin, 115 pp.