Temporal Dynamics of Early-Phase Transmission of Yersinia pestis by Unblocked Fleas: Secondary Infectious Feeds Prolong Efficient Transmission by Oropsylla montana (Siphonaptera: Ceratophyllidae)

Abstract

Plague, a flea-borne zoonotic disease, is characterized by rapidly spreading epizootics. Rate of infectious spread is thought to be related to daily biting rate of the vector, the extrinsic incubation period, vector efficiency, and the duration of infectivity. A recent study of Oropsylla montana (Baker) (Siphonaptera: Ceratophyllidae), the primary vector of Yersinia pestis (Yersin) to humans in North America, revealed that this flea feeds readily on a daily basis, has a very short extrinsic incubation period, and efficiently transmits plague bacteria for at least 4 d postinfection (p.i.). Earlier studies based on fleas receiving a single infectious bloodmeal showed that transmission efficiency wanes after 4 d p.i. In our study, we simulate a naturally occurring scenario in which fleas are exposed repeatedly to septicemic hosts, and we evaluate vector efficiency of O. montana 6-9 d after the initial infectious bloodmeal for 1) fleas given a "booster" infectious bloodmeal 5 d after initial exposure and 2) fleas that received an uninfected maintenance bloodmeal 5 d p.i. Transmission of Y. pestis was not observed beyond 7 d after initial exposure in the fleas that received a single infectious bloodmeal, whereas fleas given a booster infectious bloodmeal could transmit throughout the 9-d duration of the study. The proportion of flea pools transmitting Y. pestis was significantly higher for fleas receiving multiple, rather than single infectious bloodmeals. Surprisingly, transmission success was not directly related to bacterial loads in fleas. Our data indicated that the duration of time over which O. montana reliably transmitted plague bacteria was longer than previously thought, and this may help to explain rapid rates of epizootic spread.