Pathogen Persistence in the Environment and Insect-Baculovirus Interactions: Disease-Density Thresholds, Epidemic Burnout, and Insect Outbreaks

Abstract

Classical epidemic theory focuses on directly transmitted pathogens, but many pathogens are instead transmitted when hosts encounter infectious particles. Theory has shown that for such diseases pathogen persistence time in the environment can strongly affect disease dynamics, but estimates of persistence time, and consequently tests of the theory, are extremely rare. We consider the consequences of persistence time for the dynamics of the gypsy moth baculovirus, a pathogen transmitted when larvae consume foliage contaminated with particles released from infectious cadavers. Using field-transmission experiments, we are able to estimate persistence time under natural conditions, and inserting our estimates into a standard epidemic model suggests that epidemics are often terminated by a combination of pupation and burnout, rather than by burnout alone as predicted by theory. Extending our models to allow for multiple generations, and including environmental transmission over the winter, suggests that the virus may survive over the long term even in the absence of complex persistence mechanisms, such as environmental reservoirs or covert infections. Our work suggests that estimates of persistence times can lead to a deeper understanding of environmentally transmitted pathogens, and illustrates the usefulness of experiments that are closely tied to mathematical models.

Induced plant defenses, host–pathogen interactions, and forest insect outbreaks

“…Larvae in nature instead often consume very high doses, and they can sometimes detect and avoid infectious cadavers (38). Because of these differences, laboratory dose-response experiments often cannot be used to predict the effects of plant defenses on baculovirus infection rates in the field (23).…”

“…1-4, integrated for 56 d, the approximate length of virus epizootics in gypsy moth populations (38). The normally distributed random variate e n , which has mean 0 and standard deviation σ, allows for stochastic effects of weather, an important source of stochasticity in insect populations (43).…”

“…The term 1 − 2abNn ðb 2 + N 2 n Þ represents the fraction of insects surviving predation, as determined by a Type III functional response (6). The parameter ϕ is the overwintering impact of virus produced in generation n, including both survival and the relative susceptibility of hatchlings (38), while γ is the survival rate of virus produced in earlier generations. To allow for effects of the induced defense D n on virus transmission in generation n, we set the variability parameter in the epizootic Eqs.…”

Combining principal component analysis with parameter line-searches to improve the efficacy of Metropolis–Hastings MCMC

“…We would therefore expect that natural selection would favor virus strains with shorter speeds of kill, because the cost of producing fewer virus particles appears to be very low. In nature, however, the virus is rapidly rendered inactive by ultraviolet light (Fuller et al 2012), and so consumed doses of infectious virus may often be quite small. The slow speed of kill of this virus may therefore be an adaptation to high virus-inactivation rates, because slow-killing virus strains produce large numbers of particles that help to reduce the risk that all particles will be inactivated (Shapiro et al 2002).…”

An empirical test of the role of small-scale transmission in large-scale disease dynamics

“…Epizootics are terminated by larval pupation, or by reductions in host density that are so severe that the probability of transmission is extremely low (Fuller et al, 2012). The virus then 168 survives until the next spring by contaminating egg masses, although survival on the forest floor may also play a role (Thompson and Scott, 1979).…”