We evaluated the effects of the protozoan parasite Ophryocystis elektroscirrha on the survival and reproduction of monarch butterflies. Because larvae in natural populations are likely to experience a wide range of natural parasite population densities, we examined the effects of increasing spore density (0, 10, 100, or 1000 spores per larva) on host fitness. Parasites had little effect on monarch survival or reproduction, except at the highest dose. Monarchs inoculated with 1000 spores per larva had decreased survival to eclosion, and this effect was more severe when larvae were inoculated at an earlier stage (first versus third instar). Monarchs inoculated with higher spore densities also emerged with smaller wingspans and lower body mass than noninoculated adults. Infection with the highest dose of O. elektroscirrha led to decreased male lifespan and reproductive success, but females infected with O. elektroscirrha did not experience a significant decline in lifetime fecundity. However, heavily infected females in outdoor enclosures were less active than uninfected females and gained weight during their adult lifespan. Among samples of adult monarchs captured in natural populations, parasite loads were associated with butterfly condition and activity. Heavily infected adults captured breeding in western North America and southern Florida were smaller than uninfected monarchs. Among overwintering adults in Mexico and California, mating activity was positively associated with higher parasite loads. In addition, the proportion of adults with low and intermediate spore loads (as opposed to no spores) was higher among adults with greater wing tatter and scale loss. Our findings of minor effects of O. elektroscirrha on the survival and reproduction of monarch butterflies are consistent with the expectation that maternally transmitted parasites should have little or no effect on host fitness compared with horizontally transmitted parasites. However, because our laboratory studies demonstrated that monarchs exposed to the highest parasite density experienced decreased larval survival, smaller adult size, and shorter adult lifespans, additional transmission routes are likely to be important for parasite maintenance in natural populations. Copyright 1999 Academic Press.