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Mosquito-borne arboviral epidemics tend to strike without warning. The driving force for these epidemics is a combination of biotic (vector, amplification host, and virus) and abiotic (meteorological conditions, especially rainfall and temperature) factors. Abiotic factors that facilitate the synchronization and interaction of vector and amplification host populations favor epidemic amplification and transmission. In Florida, epidemics of St. Louis encephalitis (SLE) virus (family Flaviviridae, genus Flavivirus, SLEV) have been preceded by major freezes one or two winters before the onset of human cases. Here, we analyze the relationship between severe winter freezes and epidemic SLEV transmission in peninsular Florida and show that there is a significant relationship between the transmission of SLEV and these severe freezes. We propose that by killing cold-sensitive understory vegetation in the mid-peninsular region of Florida, freezes enhance the reproductive success of ground-feeding avian amplification hosts, especially mourning doves and common grackles. In conjunction with other appropriate environmental signals, increased avian reproductive success may enhance SLEV and West Nile (WN) virus amplification and result in SLE and WN epidemics during years when all of the biological cycles are properly synchronized. The knowledge that winter freezes in Florida may enhance the amplification and epidemic transmission of SLE and WN viruses facilitates arboviral tracking and prediction of human risk of SLE and WN infection during the transmission season.

The accurate forecasting and tracking of arboviral transmission is becoming increasingly critical for the early recognition and management of arboviral epidemics. Meteorological factors, especially rainfall and temperature, drive arboviral epidemics, but monitoring rainfall and temperature alone is not predictive of increased levels of vector-borne disease transmission. In Florida, model simulations of water table depth (WTD) provide a measure of drought, and they have been shown to provide an accurate forecast of arboviral transmission. Here, we tracked WTD in two peninsular Florida regions where focal West Nile virus (family Flaviviridae, genus Flavivirus, WNV) transmission was reported during 2004 and 2005. We compared the resulting WTD profiles with historical WTD simulations for Indian River County (IRC), FL, where two peninsular Florida St. Louis encephalitis virus epidemics had their epicenters in 1977 and 1990. In both of the regions where focal WNV transmission was reported during 2004 and 2005, the local WTD profiles approached the 1977 and 1990 IRC WTD profiles; however, differences in the local temporal sequence of hydrologic conditions were observed. These differences seem in part to explain why the focal WNV transmission during 2004 and 2005 failed to reach epidemic levels in peninsular Florida. These findings suggest that hydrologic monitoring, specifically WTD, may help determine the geographic extent, timing, and intensity of WNV transmission. We speculate that a more precise sequence of drought and wetting, including a secondary summer drying and wetting cycle, as occurred in IRC during 1977 and 1990, may provide the optimal hydrologic conditions for the expansion of an arbovirus outbreak from focal to epidemic. This study documents that monitoring hydrologic conditions, along with vector, avian amplification host, and virus population data, increases our ability to track and predict significant levels of arboviral transmission.

Mosquitoes and mosquitoborne disease transmission are sensitive to hydrologic variability. If local hydrologic conditions can be monitored or modeled at the scales at which these conditions affect the population dynamics of vector mosquitoes and the diseases they transmit, a means for monitoring or modeling mosquito populations and mosquitoborne disease transmission may be realized. We review how hydrologic conditions have been associated with mosquito abundances and mosquitoborne disease transmission and discuss the advantages of different measures of hydrologic variability. We propose that the useful application of any measure of hydrologic conditions requires additional consideration of the scales for both the hydrologic measurement and the vector control interventions that will be used to mitigate an outbreak of vectorborne disease. Our efforts to establish operational monitoring of St. Louis encephalitis virus and West Nile virus transmission in Florida are also reviewed.

We show that the spatial-temporal variability of human West Nile (WN) cases and the transmission of West Nile virus (WNV) to sentinel chickens are associated with the spatial-temporal variability of drought and wetting in southern Florida. Land surface wetness conditions at 52 sites in 31 counties in southern Florida for 2001-2003 were simulated and compared with the occurrence of human WN cases and the transmission of WNV to sentinel chickens within these counties. Both WNV transmission to sentinel chickens and the occurrence of human WN cases were associated with drought 2-6 mo prior and land surface wetting 0.5-1.5 mo prior. These dynamics are similar to the amplification and transmission patterns found in southern Florida for the closely related St. Louis encephalitis virus. Drought brings avian hosts and vector mosquitoes into close contact and facilitates the epizootic cycling and amplification of the arboviruses within these populations. Southern Florida has not recorded a severe, widespread drought since the introduction of WNV into the state in 2001. Our results indicate that widespread drought in the spring followed by wetting during summer greatly increase the probability of a WNV epidemic in southern Florida.

Using a dynamic hydrology model, we simulated land surface wetness conditions at 42 sites in 28 counties in southcentral Florida from 1990 to 1998 and compared these simulations with the incidence of human cases of St. Louis encephalitis (SLE) within these counties. Within counties, drought four months prior and wetting one-half month prior were significantly associated with human cases of SLE. Simulated land surface wetness conditions resolved transmission loci in both space and time, and May drought was significantly associated with the subsequent occurrence of human SLE cases. These findings are consistent with previous results associating simulated land surface wetness conditions with the transmission of SLE virus as measured in sentinel chickens, and support our working hypothesis that springtime drought facilitates SLE virus amplification in mosquito and wild bird populations.

Disease transmission forecasts can help minimize human and domestic animal health risks by indicating where disease control and prevention efforts should be focused. For disease systems in which weather-related variables affect pathogen proliferation, dispersal, or transmission, the potential for disease forecasting exists. We present a seasonal forecast of St. Louis encephalitis virus transmission in Indian River County, Florida. We derive an empiric relationship between modeled land surface wetness and levels of SLEV transmission in humans. We then use these data to forecast SLEV transmission with a seasonal lead. Forecast skill is demonstrated, and a real-time seasonal forecast of epidemic SLEV transmission is presented. This study demonstrates how weather and climate forecast skill-verification analyses may be applied to test the predictability of an empiric disease forecast model.

We analyzed the prevalence of hemagglutination inhibition (HI) antibodies to St. Louis encephalitis (SLE) virus in wild birds during the 1990 SLE epidemic in Indian River County. The initial presence of SLE HI antibody was associated significantly with modeled drought 15 wk prior, wetting conditions 1 wk prior, and the emergence of the Florida SLE virus vector, Culex nigripalpus, 5 wk prior. Our findings indicated that three factors conspired to create the 1990 epidemic: (1) a large population of susceptible wild birds; (2) severe springtime drought, which facilitated amplification of the SLE virus among the Cx. nigripalpus and a portion of the wild bird population; and (3) continued rainfall and wetting of the land surface in the summer and early fall, which sustained a large, host-seeking Cx. nigripalpus population. The continued biting and reproductive activity of Cx. nigripalpus maintained epizootic transmission throughout the summer and early fall in Indian River County. The high level of SLE virus amplification resulted in spillover transmission to humans. We hypothesize that without the continued reproductive activity of the vector mosquito, brought about by excessive summer and fall wetness, the unprecedented SLE virus amplification and consequent transmission to humans would not have been realized in 1990.

We used a dynamic hydrology model to simulate water table depth (WTD) and quantify the relationship between Saint Louis encephalitis virus (SLEV) transmission and hydrologic conditions in Indian River County, Florida, from 1986 through 1991, a period with an SLEV epidemic. Virus transmission followed periods of modeled drought (specifically low WTDs 12 to 17 weeks before virus transmission, followed by a rising of the water table 1 to 2 weeks before virus transmission). Further evidence from collections of Culex nigripalpus (the major mosquito vector of SLEV in Florida) suggests that during extended spring droughts vector mosquitoes and nestling, juvenile, and adult wild birds congregate in selected refuges, facilitating epizootic amplification of SLEV. When the drought ends and habitat availability increases, the SLEV-infected Cx. nigripalpus and wild birds disperse, initiating an SLEV transmission cycle. These findings demonstrate a mechanism by which drought facilitates the amplification of SLEV and its subsequent transmission to humans.