The in vitro and in situ immune responses of carp Cyprinus carpio to Ichthyophthirius multifiliis were investigated in order to characterise the immune mechanisms involved in protection. 'O' group and adult carp were immunised against I.multifiliis by controlled infection procedures. Sterile immunity was not achieved; theronts were observed to penetrate the skin of immunised fish, although in the majority of cases this did not lead to successful trophozoite establishment. It was concluded that most parasites prematurely exited the epidermis of immunised fish within two hours of penetration as an active survival strategy. Trophozoites remaining in immunised fish beyond two hours post infection were able to complete normal development. Serum from carp immunised against I.multifiliis displayed specific in vitro theront immobilising activity, and antibody was detected against parasite ciliary membranes and mucocyst organellae; similar activity was not detected in cutaneous mucus. Significant amounts of antibody could not be located at the immediate host/parasite interface of trophozoites in situ in immune skin; prevention of antibody binding may be achieved by means of a mucocyst-derived "sheath" around the parasite and the formation of a layer of necrotic host tissue debris. Parasite development in immunised fish initiated a localised cellular infiltration, predominated by type III granulocytes ("basophils'') and mast cell-like cells, the activity of which may augment further cellular and humoral infiltration. Sites of premature parasite exit from the epidermis of immunised fish were infiltrated by actively phagocytic cells, predominantly macrophages, probably in response to localised antibody/antigen complex deposition. Pronephric leucocytes of immunised fish displayed greater in vitro non-specific phagocytic activity than cells of carp naive to I.multifiliis; the relevance of this to enhanced antigen uptake in immunised fish is discussed. Based on results of the present study, a model for the Mode of protection in fish against I.multifiliis is proposed.