Aquatic Invertebrates of Montana

Tubifex and the Whirling Disease Connection

• 1995. Upenskaya, A.V. Alternation of Actinosporean and Myxosporean phases in the life cycle of Zschokkella nova (Myxozoa). Journal of Eukaryotic Microbiology 42(6): 665-668.

  Abstract: Experimental evidence has been gathered to show that the life cycle of the myxozoan gallbladder parasite Zschokkella nova Klokacewa, 1914, which infects the fish Carassius carassius, has a complex life cycle with alternation of two hosts (fish and Oligochaeta) and two developmental phases (myxosporean and actinosporean). The gut epithelium of the oligochaete, Tubifex tubifex, exposed experimentally to Z. nova, obtained from C. carassius, became infected with organisms resembling Actinosporea. The spore structure and cube-like network of the interconnected spores is reminiscent of Siedleckiella silesica Janiszewska, 1952, although the spores are very different in size and number of sporoplasm nuclei. The life cycle of Z. nova resembles that of the whirling disease agent Myxosoma cerebralis described by Wolf and Markiw, which also alternates between fish and oligochaete hosts.

• 1994. Kent, M.L. L. Margolis and J.O. Corliss. The demise of a class of protists: Taxonomic and nomenclature and revisions proposed for the protist phylum Myxozoa Grasse, 1970. Canadian Journal of Zoology 72(5): 932-937.

  Abstract: The phylum Myxozoa has been considered to comprise two classes, Myxosporea Butschli, 1881 (primarily of fishes) and Actinosporea Noble in Levine et al., 1980 (primarily of aquatic oligochaetes). About 10 years ago it was demonstrated that the life cycle of Myxobolus cerebralis Hofer, 1903 (Myxobolidae: Platysporina) of salmonid fishes requires transformation of the myxosporean into an actinosporean stage in the oligochaete worm Tubifex tubifex (Tubificidae), and that the stage infective to fish is the actinosporean spore. This type of two-host life cycle has now been demonstrated or strongly implicated for 14 myxosporean species, belonging to 6 genera in 4 families. In light of these findings, the taxonomy of the Myxozoa is revised. We propose the following: suppression of the newer class Actinosporea and the order Actinomyxidia Stolc, 1899; and suppression of all families in the Actinosporea except Tetractinomyxidae. This family and its one genus, Tetractinomyxon Ikeda, 1912, are transferred to the order Multivalvulida Shulman, 1959 (Myxosporea). We also propose that actinosporean generic names be treated as collective-group names, thus they do not compete in priority with myxosporean generic names. Triactinomyxon dubium Granata, 1924 and Triactinomyxon gyrosalmo Wolf and Markiw, 1984 are suppressed as junior synonyms of Myxobolus cerebralis. The myxosporean stage of no other previously named actinosporean has been identified. Other actinosporean species are therefore retained as species inquirendae until their myxosporean stages are identified. A revised description of the phylum Myxozoa is provided that includes our proposed taxonomic and nomenclatural changes.

• 1992. Lom, J. I. Dykova. Fine structure of Triactinomyxon early stages and sporogony: Myxosporean and actinosporean features compared. Journal Of Protozoology 39(1): 16-27.

  Abstract: The first ultrastructural study of the actinosporean genus Triactinomyxon was carried out on Triactinomyxon legeri from the intestinal epithelium of Tubifex tubifex. The developmental cycle starts with bi- and uninucleate cells. We propose that these cells may be an early proliferative phase of the cycle and may unite to give rise to the four-cell stage, initiating pansporoblast formation. Valvogenic cells transform in the long stylus and anchor-like projections of the spore. In the capsulogenic cells, the primordium of the polar capsules originates as a simple, dense, club-shaped structure not observed in other actinosporeans. In all other respects, actinosporean ultrastructure follows more or less similar patterns. Comparison of actinosporean and myxosporean species gives evidence of considerable structural similarity, exemplified in both classes by the occurrence of cell junctions in their multicellular spores, identical polar capsules and their morphogenesis, cell-in-cell condition, pansporoblast formation, and presence of dense bodies (sporoplasmosomes) primarily in the sporoplasm. This unity of patterns speaks in favor of the postulated actinosporean-myxosporean transformation, which warrants further study.

• 1991. El Matbouli, M. and R.W. Hoffmann. Effects of freezing, aging, and passage through the alimentary canal of predatory animals on the viability of Myxobolus cerebralis spores. Journal Of Aquatic Animal Health 3(4): 260-262.

  Abstract: In transmission experiments with tubificids Tubifex tubifex as primary hosts and fry of rainbow trout Oncorhynchus mykiss as secondary hosts, it was shown that Myxobolus cerebralis spores can tolerate freezing at -20 degree C for at least 3 months, aging in mud at 13 degree C for at least 5 months, and passage through the guts of northern pike Esox lucius or mallards Anas platyrhynchos without loss of infectivity.

• 1989 M. El-Matvouli and R. Hoffmann. Experimental transmission of two Myxobolus spp. developing bisporogeny via tubificid worms. Parasitol Res. 75:461-464. Abstract: Spores of Myxobolus cotti El-Matbouli and Hoffmann 1987 and M. cerebralis Hofer 1903 (fresh or after 5 months in mud) are taken in by tubifex worms and develop in their gut epithelium cells into actinosporea of the genus Triactinomyxon. Triactinomyxon deriving from M. cotti differ distinctly from those derived from M. cerebralis in morphology and the number of sporozoites in the epispore. It could be shown that Triactinomyxon spores infect fish either via the water (bullhead, rainbow trout) or by feeding of infected tubifex (rainbow trout), developing into Myxobolus spores in central nervous tissue (bullhead) or cartilage (rainbow trout). Fresh or ripened spores of M. cotti and M. cerebralis were not infectious for bullheads or rainbow trout, respectively. The results of our experiments confirm the hypothesis that the life cycle of M. cotti and M. cerebralis includes an intermediate host and a metamorphosis into actinosporea of the genus Triactinomyxon.
  1. This paper firmly established the role of Tubifex in transforming Myxosporea spores into actinosporean spores before fish infection was possible.
  2. Transformation in the worm to free swimming actinosporean spores required 94 days .
  3. Direct contact with the worms is not necessary for fish infection to occur.
  4. They obtained essentially identical resutls for a sculpin parasite Myxobolus cotti.
• 1987. Hamilton, A.J. and E.U. Canning. Studies on the proposed role of Tubifex tubifex (Muller) as an intermediate host in the life cycle of Myxosoma cerebralis (Hofer, 1903). Journal of Fish Diseases. 10:145-151. Abstract: In a recently proposed hypothesis for the transmission of Myxosoma cerebralis, the causative agent of salmonid whirling disease, it was suggested that there was a developmental cycle in tubificid worms culminating in actinosporean spores, which were infective to the fish. Results are presented here which do not support the actinosporean involvement in the life cycle. On addition of M. Cerebralis spores to Tubifex tubifex colonized in sterilized medium, no significant change in the prevalence of Triactinomyxon dubium (i.e. T. Gyrosalmo) was found. Although it is shown that these worms are capable of ingesting M. Cerebralis spores, neither hatching of the spores nor further development within the worm has been observed. Field observations on the distribution of actinosporean species show no obvious correlation between the occurrence of T. Dubium and M. cerebralis.
• 1986. Wolf, K., M.E. Markiw and J.K. Hiltunen. Salmonid whirling disease: Tubifex tubifex (Muller) identified as the essential oligochaete in the protozoan life cycle. Journal of Fish Diseases. 9: 83-85.
• 1983. Markiw, M.E. and K. Wolf. Myxosoma cerebralis (Myxozoa: Myxosporea) etiologic agent of salmonid whirling disease requires tubificid worm (Annelida: Oligochaeta) in its life cycle. Journal of Protozoology. 30: 561-564. Abstract: Studies of the life cycle of Myxosoma cerebralis showed that development of infectivity did not occur endogenously but that the spore "aging" process required participation of an aquatic tubificid oligochaete. Data suggestive of such involvement were derived from trials in which spores were "aged" in an array of inert, sterilized, pasteurized, or natural aquatic substrates and from examination of aquatic soils from trout hatcheries in which whirling disease was epizootic. The role of the aquatic oligochaete was confirmed two ways. First, signs of whirling disease developed, and M. cerebralis spores were produced in young rainbow trout (Salmo gairdneri ) that had been fed oligochaetes harvested from pond soil taken from two hatcheries where whirling disease was epizootic. Second, when containers of pasteurized soil were populated with four genera of oligochaetes - Aeolosoma, Dero, Stylaria, or Tubifex - from a biological supply house, or with tubificid worms from trout hatcheries free of whirling disease, and then seeded with M. cerebralis spores and "aged" for 4 months, whirling disease occurred only in trout held with Tubifex and with hatchery tubifids.