Biology 625
ANIMAL PARASITOLOGY
Fall semester lecture note outline

Updated: 09 March 2005

1. The systematic position of the Myxozoa are not precisely known. Some authors have grouped them with the Cnidaria whereas others have not
2. Typical features of the Cnidaria
   1. Aquatic; most marine
   2. Radial symmetry
   3. Most with gastrovascular cavity
   4. Most have tentacles at some stage, which are derived as extensions of body wall
   5. Nematocysts (stinging cells) in many species
   6. Most species with an alternation of generations (asexual polyploid and sexual medusa generations), although in many species one or the other stage may be reduced significantly or even absent
   7. Three traditional classes in the phylum, two of which (the hydrozoans and sea anemones) have parasitic members (although only a single taxon will be presented here). Exactly where the Myxozoa fit in this taxonomic scheme has not yet been fully determined, but they appear to represent a fourth distinct group (1995, J Parasitol 81: 961-967).
      1. Class: Hydrozoa (hydras; with 4 orders)
      2. Class: Schyphozoa (jellyfish; with 4 orders)
      3. Class: Anthozoa (sea anemones and corals; with 2 subclasses and about 11 orders)
3. Multiple taxa are parasitic, although only Polypodium and the myxozoa are discussed in detail below:
   1. The myxozoans (may or may not be allied with the Cnidaria) are discussed briefly below
   2. Polypodium hydriforme (not to be confused with the genus of fern that has the same name) (probably related to hydras) is a true cnidarian and is also discussed below
   3. Some larval sea anemones, for instance Peachia quinquecapitata, become parasitic (once ingested) and feed on the internal organs (stomach and gonads) of free-living hydromedusae. They then drop out of the host, settle to the bottom, and develop as free-living adults
   4. Some tiny larval cnidarians, for instance Linuche unquiculata (thimble jellyfish) in the Caribbean, can be induced to fire nematocysts by mechanical pressure (for instance, under a bathing suit). Outbreaks of dermatitis are sometimes reported March-July of some years, and has been erroneously been termed "sea lice" dermatitis.
   5. Some small anemones are parasitic on Gorgonian fans and other corals, for instance the zoanthid anemone Parazoanthus lucificum, resulting in bleaching and death of the coral
   6. Calliactis parasitica is an anemone that often attaches to the shells of hermit crabs. Although often termed parasitic, the relationship is more mutualistic

Myxozoa

1. All members of this group parasitic, most of which occur in teleost fish. Reprentatives also known from invertebrates, amphibia, and turtles
2. Siddall et al. (1995, J Parasitol 81: 961-967) provided morphologic and genetic evidence that the myxozoa were cnidarians; a distant relative of Polypodium. This hypothesis has been supported by some authors (i.e. Zrzavy et al. 1998, Cladistics 14: 249-282) whereas other authors have not reached the same conclusion (i.e. Schlegel et al. 1996, Arch Protistenkd 147: 1-9; Winnepenninckx et al. 1998, Am Zool 38: 888-906).
3. Spores of multicellular origin and are structurally and genetically metazoan
4. Each spore contains 1-more polar capsules each with a polar filament that is expelled during invasion; and 1-more sporoplasms
5. Each spore is comprised of 1, 2, 3, or rarely more valves
6. About 1200 species and nearly 50 genera known
7. Composite (hypothetical) life-cycle
   1. Earliest stages found in fish (intermediate host) are trophozoites within cells. Depending upon species, the cell type targeted will tend to be specific.
   2. Amoeboid cytoplasm eventually increases in size and nucleus undergoes repeated karyokinesis to form a plasmodium (large cytoplasmic mass with many nuclei)
   3. Plasmodia grow attached to the epithelium in the coelomic area in coelozoic forms (i.e. urinary bladder, swim bladder), or occur within tissues themselves in histozoic forms
   4. In many coelomic forms, during the winter the plasmodia (i.e. Myxobilatus microspora in urinary bladder of largemouth bass) are sheet-like. In late spring and summer, plasmodia form long, finger-like extensions, bud off so that free-floating plasmodia occur, and spores form within the fingers and buds which pass out with the urine (see 1981, J Parasitol 67: 859-865)..
   5. Some cells are destined to form spores within the plasmodia. The following represents spore formation in Henneguya exilis in channel catfish (1977, Protistologica 13: 157-167)
      1. An envelope cell encapsulates a sporogonic cell
      2. Multiple cell divisions of sporogonic cell to form 10 new cells that eventually form 2 separate spores within the envelope cell. This 2 spores from the same cells is termed "disporoblastic spore formation." Other types of spore formation occur.
         1. 4 capsulogenic cells (2 per spore; 1 per polar capsule)
         2. 4 valvulogenic cells (2 per spore; 1 per each valve)
         3. 2 sporoplasms (1 per spore)
   6. Spores liberated into environment
   7. Ingested by tubificid oligochaetes (definitive host)
   8. Polar filaments expelled, valves separate, and sporoplasm invades gut (usually, intracellular spaces between intestinal epithelial cells)
   9. Sporoplasm divides asexually, sometimes by multiple fission.
   10. Gamogony, where cells derived from different plasmodia fuse.
   11. Triactinomyxon (3 valve) spores released into the lumen of the gut
   12. Spores in water attach to fish via polar filaments; sporoplasms invade cells of primary host. Fish can also become infected by ingesting infected oligochaetes.
8. Some representative genera and species
   1. Chloromyxum trijugum in the gall bladder of centrarchids in North America
   2. Henneguya exilis in the gill filaments of channel catfish in North America
   3. Myxidium serotinum in the gall bladder of anurans in the Western hemisphere
   4. Myxobilatus mictospora in the urinary bladder of large mouth bass in North America
   5. Myxobolus cyprini in muscles of carp in Europe
   6. Myxosoma cerebralis infecting the cartilege and causing deformities in trout; introduced along with Brown trout from Europe into North America.
   7. Sphaerospora renicola in the renal tubuli of European carp
   8. Thelohanellus nikolskii in cysts on the fins of carp in Europe
9. Taxonomy of the entire myxozoan group (1984, Folia Parasitol 31: 193-205); of the Myxobolus/Myxosoma group (1991, Syst Parasitol 18: 165-186).

Polypodium hydriforme (Phylum: Cnidaria, Class: Hydrozoa)

1. You will only be required to know that this species of hydrozoan infects the eggs of sturgeon and other primitive fish. You will not need to learn the life-cycle.
2. Adapted to parasitism in oocytes of primitive fish
   1. Acipenser spp. (Acipenseridae) (sturgeon, sterlet, sevrjuga) in Europe and North America
   2. Huso spp. (Acipenseridae) (kaluga) in Russia
   3. Polyodon spathula (Polydontidae) (paddlefish) in North America
3. Parasitic stages in found in oocytes throughout oogenesis, beginning with previtellogenesis up until spawning over one year later.
4. Life cycle
   1. single cells in previtellogenic oocytes. Each cell with 2 nuclei (1 large and 1 small (haploid) nucleus closely associated with large nucleus)
   2. Nucleus of large cell begins to "engulf" smaller nucleus, and small nucleus becomes enveloped within thin layer of cytoplasm within the larger nucleus. Thus, a small cell within a larger cell. The nucleus of the small cell is haploid, whereas that of the large cell becomes polyploid (eventually, the parasite becomes diploid but it is unknown at what stage this occurs)
   3. Small cell begins to divide while within larger cell (now termed a trophamnion; essentially a nurse cell that will support development of the smaller cell). The small cell divides to form "blastomeres," and eventually a cluster of cells forms (embryo) within the hollowed out (and also growing) trophamnion.
   4. Embryo gradually elongates
   5. The embryo eventually undergoes gastrulation
   6. Nucleus of trophamnion gradually becomes reticulate
   7. Eventually, in late May to late July of the year prior to spawning, when oocytes are beginning to accumulate yolk, a planula type larva with 2 epithelial layers forms.
   8. Eggs become more pigmented (darker) and larger in size than uninfected eggs, and the egg nucleus becomes damaged by the parasitism
   9. Larva begins to elongate and undergo multiple budding, and forms a stolon in August.
   10. Stolon continues to elongate, becomes convoluted, and eventually possesses 30-40 buds
   11. Tentacles gradually form; eventually acquire nematocysts (by end of October)
   12. Development becomes arrested during winter
   13. Between March and May of following year, buds on stolons increase in size and tentacles elongate
   14. Prior to the fish spawning, stolon turns inside out; ruptures out of egg (usually in the oviduct) during spawning
   15. Thus, stolons with tentacles released into water directly
   16. Once in water, stolon fragments into pieces and continues to fragment throughout summer until organisms with 6 tentacles or less predominate
   17. As yolk reserves in stolon become depleted, each forms a mouth and feeds on small invertebrates
   18. Grow, develop more tentacles, and reproduce by binary fission; can walk on substrate using tentacles
   19. In August, male and female gonads form (female gonads form first); parthenogenesis or self-fertilization?
   20. It is thought that free-living, sexual Polypodium deposit gametophores into very young fish that still retain a yolk sac. This has been observed naturally where the parasites are seen attached to the yolk sac, head, body, tail, and fin fold of young sturgeon.
5. Review article (1994, J Parasitol 80: 1-22).