Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-08T07:30:50.851Z Has data issue: false hasContentIssue false
  • English
  • Français

First taxonomic description of multivalvulidan myxosporean parasites from elasmobranchs: Kudoa hemiscylli n.sp. and Kudoa carcharhini n.sp. (Myxosporea: Multivalvulidae)

Published online by Cambridge University Press:  12 July 2010

R. J. GLEESON ,
M. B. BENNETT  and
R. D. ADLARD
R. J. GLEESON
Affiliation:
School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, Queensland 4072, Australia Biodiversity Program, Queensland Museum, PO Box 3300, South Brisbane, Queensland 4101, Australia
M. B. BENNETT
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, Queensland 4072, Australia
R. D. ADLARD*
Affiliation:
School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, Queensland 4072, Australia Biodiversity Program, Queensland Museum, PO Box 3300, South Brisbane, Queensland 4101, Australia
*
*Corresponding author: Biodiversity Program, Queensland Museum, PO Box 3300, South Brisbane, Queensland 4101, Australia. Tel: +617 3840 7723. Fax: +617 3846 1226. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Myxosporean parasites are significant parasites of fishes not only for their apparent high diversity but also for their potential impact on fish health and/or marketability. Regardless, our knowledge of most myxosporeans, especially those found in elasmobranch hosts, is superficial. A study of multivalvulidan diversity in a range of elasmobranchs from Queensland, Western Australia and the Northern Territory (Australia) was conducted to address this knowledge gap. Specimens were collected from a total of 3 orders, 9 families and 31 species of elasmobranchs. Myxosporean infections referable to the genus Kudoa were discovered in host muscle and characterized morphologically and genetically. Both small subunit (SSU) and large subunit (LSU) rDNA sequences were used in molecular phylogenetic analyses. Kudoa spp. infected 27 of the 31 species of elasmobranchs examined, representing new records of this parasite genus in 26, of the 27, host species. Kudoids were observed in all 3 orders, and 7 out of the 9 families of elasmobranchs investigated. This paper reports the first 2 multivalvulidan species to be formally described from elasmobranchs, Kudoa hemiscylli n.sp. characterized from Hemiscyllium ocellatum (and 8 other host species) and Kudoa carcharhini n. sp. characterized from Carcharhinus cautus (and 2 other host species). Phylogenetic analyses revealed that kudoids from elasmobranchs form a separate lineage to those of teleosts, but are anchored within the overall kudoid clade.

Keywords

MultivalvulidaMyxosporeaKudoidaeKudoadiversityphylogenyelasmobranchs
Type
Research Article
Information
Parasitology , Volume 137 , Issue 13 , November 2010 , pp. 1885 - 1898
Copyright
Copyright © Cambridge University Press 2010

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

REFERENCES

Andree, K. B., El-Matbouli, M., Hoffman, R. W. and Hedrick, R. P. (1999). Comparison of 18S and ITS-1 rDNA sequences of selected geographic isolates of Myxobolus cerebralis. International Journal for Parasitology 29, 771–775. doi:10.1016/S0020-7519(99)00035-1.CrossRefGoogle ScholarPubMed
Bartholomew, J. L., Atkinson, S. D., Hallett, S. L., Lowenstine, L. J., Garner, M. M., Gardiner, C. H., Rideout, B. A., Keel, M. K. and Brown, J. D. (2008). Myxozoan parasites in waterfowl. International Journal for Parasitology 38, 1199–1207. doi:10.1016/j.ijpara.2008.01.008.CrossRefGoogle ScholarPubMed
Benz, G. W. and Bullard, S. A. (2004). Metazoan parasites and associates of chondrichthyans with emphasis on taxa harmful to captive hosts - Myxozoans. In The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and their Relatives (ed. Smith, , , M., Warmolts, , , D., Thoney, , , D. and Hueter, , , R.), pp. 379–381. Special Publication of the Ohio Biological Survey, Ohio, USA.Google Scholar
Blaylock, R. B., Bullard, S. A. and Whipps, C. M. (2004). Kudoa hypoepicardialis n.sp. (Myxozoa:Kudoidae) and associated lesions from the heart of seven perciform fishes in the northern Gulf of Mexico. Journal of Parasitology 90, 584–593.CrossRefGoogle ScholarPubMed
Burger, M. A. A. and Adlard, R. D. (2010). Four new species of Kudoa Meglitsch, 1947 (Myxosporea: Multivalvulida) from Australia with recommendations for species descriptions in the Kudoidae. Parasitology 137, 793–814. doi:10.1017/S0031182009991557.CrossRefGoogle Scholar
Burger, M. A. A., Barnes, A. C. and Adlard, R. D. (2008). Wildlife as reservoirs for parasites infecting commercial species: host specificity and a redescription of Kudoa amamiensis from teleost fish in Australia. Journal of Fish Diseases 31, 835–844. doi:10.1111/j.1365-2761.2008.00958.x.CrossRefGoogle Scholar
Burger, M. A. A., Cribb, T. H. and Adlard, R. D. (2007). Patterns of relatedness in the Kudoidae with descriptions of Kudoa chaetodoni n. sp. and K. lethrini n. sp. (Myxosporea: Multivalvulida). Parasitology 134, 669–681. doi:10.1017/S0031182006001995.CrossRefGoogle ScholarPubMed
Compagno, L., Dando, M. and Fowler, S. (2005). Sharks of the World. Princeton Field Guides. Princeton University Press, NJ, USA.Google Scholar
Diamant, A., Ucko, M., Paperna, I., Colorni, A. and Lipshitz, A. (2005). Kudoa iwatai (Myxosporea: Multivalvulida) in wild and cultured fish in the Red Sea: redescription and molecular phylogeny. Journal of Parasitology 91, 1175–1189. doi:10.1645/GE-491R.1.CrossRefGoogle ScholarPubMed
Douady, C. J., Dosay, M., Shiyii, M. S. and Stanhope, M. J. (2003). Molecular phylogenetic evidence refuting the hypothesis of Batoidea (rays and skates) as derived sharks. Molecular Phylogenetics and Evolution 26, 215–221.CrossRefGoogle ScholarPubMed
Egusa, S. (1986). The order Multivalvulida Shulman, 1959 (Myxozoa: Myxosporea): a review. Fish Pathology 21, 261–274.CrossRefGoogle Scholar
Egusa, S. and Shiomitsu, T. (1983). Two new species of the genus Kudoa (Myxosporea: Multivalvulida) from marine cultured fishes in Japan. Fish Pathology 18, 163–171.CrossRefGoogle Scholar
Friedrich, C., Ingolic, E., Freitag, B., Kastberger, G., Hohmann, V., Skofitsch, G., Neumeister, U. and Kepka, O. (2000). A myxozoan-like parasite causing xenomas in the brain of the mole Talpa europrea L., 1758. Parasitology 121, 483–492.CrossRefGoogle ScholarPubMed
Gunter, N. L., Whipps, C. M., Cribb, T. H. and Adlard, R. D. (2006). Characterisation of Kudoa monodactyli n. sp. (Myxozoa: Multivalvulida) from Monodactylus argenteus (Teleostei: Monodactylidae) from Moreton Bay, Queensland, Australia. Journal of Eukaryotic Microbiology 53, 374–378. doi:10.1111/j.15507408.2006.00115.x.CrossRefGoogle Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hammer, Ø., Harper, D. A. T. and Ryan, P. D. (2001) PAST: paleontological statistics software package for education & data analysis, version 1.74. Palaeontologia Electronica 4, 9.Google Scholar
Heulsenbeck, J. P. and Ronquist, F. (2001). Bayesian inference of phylogeny. Biometrics 17, 754–755.Google Scholar
Heupel, M. R. and Bennett, M. B. (1996). A myxosporean parasite (Myxosporea: Multivalvulida) in the skeletal muscle of epaulette sharks, Hemiscyllium ocellatum (Bonnaterre), from the Great Barrier Reef. Journal of Fish Diseases 19, 189–191.CrossRefGoogle Scholar
Hillis, D. M. and Dixon, M. T. (1991). Ribosomal DNA – molecular evolution and phylogenetic inference. Quarterly Review of Biology 66, 410–453.CrossRefGoogle ScholarPubMed
Iverson, E. S. and van Meter, N. N. (1967). A new myxosporidian (Sporozoa) infecting the Spanish mackerel. Bulletin of Marine Science 17, 268–273.Google Scholar
Kent, M. L., Andree, K. B., Bartholomew, J. L., El-Matbouli, M., Desser, S. S., Devlin, R. H., Feist, S. W., Hedrick, R. P., Hoffmann, R. W., Khattra, J., Hallett, S. L., Lester, R. J. G., Longshaw, M., Palenzeula, O., Siddall, M. E. and Xiao, C. (2001). Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 48, 395–413.CrossRefGoogle ScholarPubMed
Kovaljova, A. A., Shulman, S. S. and Yakovlev, V. N. (1979). Myxosporidia of the genus Kudoa (Myxosporidia, Multivalvulida) of the Atlantic Ocean basin. Trudy Zoologicheskogo Instituta Akademii Nauk SSSR 87, 42–64.Google Scholar
Kudo, R. (1920). Studies on the Myxosporidia: A synopsis of genera and species of Myxosporidia. Illinois Biological Monographs 5, 1–265.Google Scholar
Last, P. R. and Stevens, J. D. (2009). Sharks and Rays of Australia. 2nd Edn. C.S.I.R.O. Publishing, Melbourne, Australia.Google Scholar
Lom, J. and Arthur, J. R. (1989). A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases 12, 151–156. doi:10.1111/j.13652761.1989.tb00287.x.CrossRefGoogle Scholar
Lom, J. and Dyková, I. (1992). Protozoan Parasites of Fishes. Developments in Aquaculture and Fisheries Sciences. Elsevier, Amsterdam, The Netherlands.Google Scholar
Lom, J. and Dyková, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 1–36.CrossRefGoogle ScholarPubMed
Moran, J. D. W., Whitaker, D. J. and Kent, M. L. (1999). A review of the myxosporean genus Kudoa Meglitsch, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172, 163–196.CrossRefGoogle Scholar
O'Donoghue, P. J. and Adlard, R. D. (2000). Catalogue of protozoan parasites recorded in Australia. Memoirs of the Queensland Museum 45, 1–163.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Prunescu, C-C., Prunescu, P., Pucek, Z. and Lom, J. (2007). The first finding of myxosporean development from plasmodia to spores in terrestrial mammals: Soricimyxum fegati gen. et sp. n. (Myxozoa) from Sorex araneus (Soricomorpha). Folia Parasitologica 54, 159–164.CrossRefGoogle Scholar
St-Hilaire, S., Hill, M., Kent, M. L., Whitaker, D. J. and Ribble, C. (1997). A comparative study of muscle texture and intensity of Kudoa thyrsites infection in farm-reared Atlantic salmon Salmo salar on the Pacific coast of Canada. Diseases of Aquatic Organisms 31, 221–225.CrossRefGoogle Scholar
Stoffregen, D. A. and Anderson, W. I. (1990). A myxosporidian parasite in the skeletal muscle of a black-tip reef shark, Carcharhinus melanopterus (Quoy and Gaimard, 1824). Journal of Fish Diseases 13, 549–552.CrossRefGoogle Scholar
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis using Parsimony (*and other Methods), 4th Edn. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (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
Whipps, C. M., Adlard, R. D., Bryant, M. S. and Kent, M. L. (2003 a). Two unusual myxozoans, Kudoa quadricornis n. sp. (Multivalvulida) from the muscle of goldspotted trevally (Carangoides fulvoguttatus) and Kudoa permulticapsula n. sp. (Multivalvulida) from the muscle of spanish mackerel (Scomberomorus commerson) from the Great Barrier Reef, Australia. Journal of Parasitology 89, 168–173. doi:10.1645/00223395(2003)089[0168:TUMKQN]2.0.CO;2.CrossRefGoogle Scholar
Whipps, C. M., Adlard, R. D., Bryant, M. S., Lester, R. J. G., Findlay, V. and Kent, M. L. (2003 b). First report of three Kudoa species from Eastern Australia: Kudoa thyrsites from Mahi mahi (Coryphaena hippurus), Kudoa amamiensis and Kudoa minithyrsites n. sp from Sweeper (Pempheris ypsilychnus). Journal of Eukaryotic Microbiology 50, 215–219. doi:10.1111/j.1550-7408.2003.tb00120.x.CrossRefGoogle Scholar
Whipps, C. M., Grossel, G., Adlard, R. D., Yokoyama, H., Bryant, M. S., Munday, B. L. and Kent, M. L. (2004). Phylogeny of the Multivalvulida (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. Journal of Parasitology 90, 618–622. doi:10.1645/GE-153R.CrossRefGoogle ScholarPubMed
Whipps, C. M. and Kent, M. L. (2006). Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). Journal of Eukaryotic Microbiology 53, 364–373. doi:10.1111/j.1550-7408.2006.00114.x.CrossRefGoogle ScholarPubMed
Winchell, C. J., Martin, A. P. and Mallatt, J. (2004). Phylogeny of elasmobranchs based on LSU and SSU ribosomal RNA genes. Molecular Phylogenetics and Evolution 31, 214–224.CrossRefGoogle ScholarPubMed
Yokoyama, H. (2003). A review: Gaps in our knowledge on myxozoan parasites of fishes. Fish Pathology 38, 125–136.CrossRefGoogle Scholar
Yokoyama, H. and Masuda, K. (2001). Kudoa sp (Myxozoa) causing a post-mortem myoliquefaction of North-Pacific giant octopus Paroctopus dofleini (Cephalopoda: Octopodidae). Bulletin of the European Association of Fish Pathologists 21, 266–268.Google Scholar