Hypothesis: dynamics of classical malaria epidemics show Plasmodium falciparum's survival strategy.

Areas of marginal transmission can generate enormous lethal falciparum malaria epidemics when factors favoring the parasite shift only slightly. Although usually described in terms of vectorial capacity, medical scientists working in India in the early 20th century came to the conclusion that "an epidemic of relapses" was the key triggering event of malaria epidemics. This explanation has been largely discarded, because the biology of Plasmodium falciparum recrudescence has since been differentiated from P. vivax relapse. Using data from the Punjab in 1908 and Ceylon in 1934-1935, the genesis of malaria epidemics has been re-examined to inform current control efforts. The epidemics were focused geographically depending on recent rainfall or drought. Epidemics arose very suddenly and simultaneously in several places. Malaria spleen surveys indicated very little recent malaria transmission, and blood smears showed very few gametocytes just before the epidemic. Population stress as indicated by high grain prices because of a poor harvest caused by drought the previous year was a risk factor for malaria epidemics. Although increased female Anopheline survival because of increased humidity played an important part in the magnification of the epidemic, it does not explain its genesis. Human population stress triggering a shift toward gametocytogenesis is hypothesized as the key initiation factor for malaria epidemics. Its evolutionary significance may be that it allows the parasite to match the tropical agricultural cycle. © The American Society of Tropical Medicine and Hygiene.