Zoospores of the nematode-parasitic Catenaria anguillulae (Chytridiomycota) were studied by videomicroscopy in sealed films of water on microscope slides in the presence or absence of freeze-inactivated nematodes (Panagrellus redivivus). Zoospores swam for more than 1 h at a mean velocity of 104 μm s−1, interspersed with repeated phases (1–2 min) of amoeboid crawling on glass or nematode surfaces. They were attracted to and encysted near the mouth, excretory pore, and anus of nematodes, or eventually encysted at random on glass and nematode surfaces. The single posterior flagellum was immobile during amoeboid crawling but resumed rapid beating when the last pseudopodium was being retracted. Zoospores encysted by adhesion of the anterior of an amoeboid cell to a surface; then the cell posterior was raised above the anterior so that the flagellum projected perpendicular to the surface, and the flagellum was retracted by rotation of the cell contents. Cysts germinated within 20–60 min by a narrow germ-tube at the site of adhesion. The germ-tube grew a short distance, then formed an intercalary vesicle into which the cyst contents emptied by expansion of a cyst vacuole. In several cases the germ-tube penetrated a nematode and formed the vesicle inside the host. Rhizoids or assimilative hyphae developed from the vesicle or by growth of the germ-tube tip. An increasing proportion of zoospores that remained motile after 1 h in water films had a globose body in contrast to the normal elongated form. This seemed to be caused by damage during repeated transitions between the amoeboid and swimming phases, because pseudopodia sometimes remained firmly attached to a glass surface.

C. anguillulae showed consistent orientation (polarity) of zoospore encystment and cyst germination. This parallels the behaviour of other zoosporic fungi or fungus-like organisms (Plasmodiophora brassicae, Rozella allomycis, Pythium, Phytophthora and Saprolegnia spp.) suggesting that it is a common feature of zoosporic parasites. Surface-recognition for encystment by C. anguillulae was mediated by the zoospore soma, not the flagellum. In addition, we redefine the early development of C. anguillulae, including flagellar retraction by rotation of cell contents, non-specific adhesion of zoospores and cysts to surfaces, and evacuation of cyst contents into a vesicle from which further growth occurs.