Influence of delayed density and ultraviolet radiation on caterpillar baculovirus infection and mortality.

Infectious disease is an important potential driver of population cycles but must occur through delayed density-dependent infection and resulting fitness effects. Delayed density-dependent infection by baculoviruses can be caused by environmental persistence of viral occlusion bodies (OBs), which can be influenced by environmental factors. Specifically, ultraviolet radiation is potentially important in reducing the environmental persistence of viruses by inactivating OBs. Delayed density-dependent viral infection has rarely been observed empirically at the population level although theory predicts that it is necessary for pathogens to drive population cycles. Similarly, field studies have not examined the effects of ultraviolet radiation on viral infection rates in natural animal populations. We tested if viral infection is delayed density-dependent with the potential to drive cyclic dynamics and if ultraviolet radiation influences viral infection levels. We censused 18 Ranchman's tiger moth (Arctia virginalis) populations across 9° of latitude over 2 years and quantified the effects of direct and delayed density and ultraviolet radiation on proportion infected by baculovirus, infection severity and survival to adulthood. Caterpillars were collected from field populations and reared in the laboratory. Baculovirus has not previously been described infecting A. virginalis, and we used genetic methods to confirm the identity of the virus. We found that proportion infected, infection severity and survival to adulthood exhibited delayed density dependence. Ultraviolet radiation in the previous summer decreased infection severity, which increased caterpillar survival probability. Structural equation modelling indicated that the effect of lagged density on caterpillar survival was mediated through proportion infected and infection severity and was 2.5-fold stronger than the indirect effect of ultraviolet. We successfully amplified polh, lef-8 and lef-9 viral genes from caterpillars, and BLAST results confirmed that the virus was a nucleopolyhedrovirus. Our findings provide clear evidence that delayed density-dependent mortality can arise through viral infection rate and severity in insects, which supports the role of viral disease as a mechanism, among others, that may drive insect population cycles. Furthermore, our findings support predictions that ultraviolet radiation can modify viral disease dynamics in insect populations, most likely through attenuating viral persistence in the environment.

Spatial habitat heterogeneity influences host-pathogen dynamics in a patchy population of Ranchman's tiger moth.

Host-pathogen dynamics are influenced by many factors that vary locally, but models of disease rarely consider dynamics across spatially heterogeneous environments. In addition, theory predicts that dispersal will influence host-pathogen dynamics of populations that are linked, although this has not been examined empirically in natural systems. We examined the spatial dynamics of a patchy population of tiger moths and its baculovirus pathogen, in which habitat type and weather influence dynamics. Theoretical models of host-baculovirus dynamics predict that such variation in dynamics between habitat types could be driven by a range of factors, of which we predict two are likely to be operating in this system: (1) differences in the environmental persistence of pathogens or (2) differences in host intrinsic rates of increase. We used time series models and monitored infection rates of hosts to characterize population and disease dynamics and distinguish between these possibilities. We also examined the role of host dispersal (connectivity) and weather as important contributors to dynamics, using time series models and experiments. We found that the population growth rate was higher, delayed density dependence was weaker, and long-period oscillations had lower amplitudes in high-quality habitat patches. The infection rate was higher on average in high-quality habitat, and this was likely to have been driven by higher mean population densities and no differences in pathogen persistence in different habitats (delayed density dependence). Time series modeling and experiments also showed an interactive effect of temperature and precipitation on moth population growth rates (likely caused by variation in host plant quality and quantity), and an effect of connectivity. Our results showed that spatial heterogeneity, connectivity, climate, and their interactions were important in driving host-baculovirus dynamics. In particular, our study found that connected patches and spatial heterogeneity generated differences in dynamics that only partially aligned with theoretical predictions.