Pathogen Persistence in the Environment and Insect-Baculovirus Interactions: Disease-Density Thresholds, Epidemic Burnout, and Insect Outbreaks (original) (raw)
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F1000 - Post-publication peer review of the biomedical literature, 2012
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.
2016
Mathematical models of disease outbreaks play a crucial role in guiding public health policy [1–3] and have provided critical insights into the ecological dynamics of pathogen-regulated populations [4,5]. Remarkably, the models used to describe epidemics among human populations have been quite successful at describing epizootics in many animal populations, including forest-and crop-defoliating insect pests [6] whose population dynamics are often driven by baculoviruses [7]. Given the variety of insect species affected by baculoviruses and their ubiquity in nature, these viruses may help in the development of disease models that not only increase our understanding of disease transmission in general, but directly lead to better agricultural and forestry management through environmentally benign pest control. What Are Baculoviruses? From a medical and microbiology perspective, baculoviruses
Oecologia, 1999
In 1990, natural infestations of the polyphagous vapourer moth, Orgyia antiqua (Lepidoptera: Lymantriidae) in lodgepole pine plantations in northern Scotland, were studied to ascertain the role of host foraging behaviour on the prevalence of nucleopolyhedrovirus (NPV; Baculoviridae) infection in the population. Aerial dispersal of early instar larvae (L1± L3) from the tree canopy onto heather foliage at the forest understorey, with subsequent relocation back onto the tree as late-instar larvae (L4±L6) appeared to play a signi®cant role in the development of a widespread virus epizootic in which approximately 80% of L4±L6 individuals succumbed to disease. Bioassays of foliage 1 year later showed that the distribution of NPV followed a pronounced vertical gradient through the forest canopy culminating in high concentrations of virus in the forest understorey. Experimental systems comprising potted pine trees positioned above heather bases showed that NPV infections could be acquired by early stage larvae following dispersal from the tree and feeding on the undercanopy vegetation, then translocated to the tree component for secondary transmission to susceptible tree-feeding individuals. Behavioural studies indicated that the tendency for ®rst-, secondand third-instar larvae to disperse to the understorey was probably not in¯uenced by larval density on the tree but was strongly dependent on larval instar. In contrast, the tendency for larvae to relocate from the understorey heather to the tree was aected by both larval density and larval instar, suggesting that both these factors may signi®cantly aect virus acquisition, translocation and transmission in the host population. In the present study, the heather understorey appeared to act as a pathogen reservoir in which virus could persist between host generations. Spatial heterogeneity in virus distribution combined with host foraging behaviour (dispersal and feeding) resulted in the pathogen playing a major role in host population dynamics over an extended time period (3 years). The reservoir theory is supported by the observation that similar dynamics were not observed in O. antiqua populations at neighbouring sites which lacked understorey food plants.
Spatiotemporal dynamics of insect pest population under viral infection
The interrelationship between pathogen infection and host mobility is of great importance for successful spread of disease in spatial pest population. As spread of infection depends on horizontal transmission of pathogen, there are numerous factors like susceptibility, latent period, host movement that influence overall effectiveness of the control policy. Initiation of new infection cycle depends on density of infected inoculum in the site. So, spatial movement of infected hosts during the course of infection influence the dynamics. Also, infected individuals are more vulnerable to predators and hence production of virus particles in the site depends on predation to some extent. We derive a four dimensional delayed reaction– diffusion model in one spatial dimension and compute the minimum travelling speed of transmission of infection. We show that the minimum speed is sensitive to several parameters of the system. For example , the minimum speed decreases only with increase in delay in lysis process, but otherwise it increases with increase in force of infection, diffusivity of infectives or per capita virus production. A concluding discussion with numerical simulation is presented in the end. Published by Elsevier Inc.
Virus Transmission in Gypsy Moths is not a Simple Mass Action Process
Ecology, 1996
We used the nuclear polyhedrosis virus (LdNPV) of the gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae), to test one of the basic assumptions of most models of disease dynamics, that the rate of horizontal transmission is directly proportional to the product of the densities of healthy larvae and virus. To do this we made measurements of virus transmission, using small-scale experiments in bags on red oak (Quercus rubra) foliage and field data on naturally occurring populations from a previous study. We observed a decline in the transmission constant as the densities of both healthy larvae and pathogen increased, indicating that the rate of disease transmission is not directly proportional to the product of these variables.
Environmental Persistence Influences Infection Dynamics for a Butterfly Pathogen
PloS one, 2017
Many pathogens, including those infecting insects, are transmitted via dormant stages shed into the environment, where they must persist until encountering a susceptible host. Understanding how abiotic conditions influence environmental persistence and how these factors influence pathogen spread are crucial for predicting patterns of infection risk. Here, we explored the consequences of environmental transmission for infection dynamics of a debilitating protozoan parasite (Ophryocystis elektroscirrha) that infects monarch butterflies (Danaus plexippus). We first conducted an experiment to observe the persistence of protozoan spores exposed to natural conditions. Experimental results showed that, contrary to our expectations, pathogen doses maintained high infectivity even after 16 days in the environment, although pathogens did yield infections with lower parasite loads after environmental exposure. Because pathogen longevity exceeded the time span of our experiment, we developed a ...
Host behaviour and exposure risk in an insect-pathogen interaction
Journal of Animal Ecology, 2010
1. Studies of variability in host resistance to disease generally emphasize variability in susceptibility given exposure, neglecting the possibility that hosts may vary in behaviours that affect the risk of exposure. 2. In many insects, horizontal transmission of baculoviruses occurs when larvae consume foliage contaminated by the cadavers of virus-infected conspecific larvae; so, host behaviour may have a strong effect on the risk of infection. 3. We studied variability in the behaviour of gypsy moth (Lymantria dispar) larvae, which are able to detect and avoid virus-contaminated foliage. 4. Our results show that detection ability can be affected by the family line that larvae originate from, even at some distance from a virus-infected cadaver, and suggest that cadaver-detection ability may be heritable. 5. There is thus the potential for natural selection to act on cadaver-detection ability, and thereby to affect the dynamics of pathogen-driven cycles in gypsy moth populations. 6. We argue that host behaviour is a neglected component in studies of variability in disease resistance.
Insect virus transmission: different routes to persistence
Current Opinion in Insect Science, 2015
Transmission is a fundamental process in disease ecology; however, the factors that modulate transmission and the dynamical and evolutionary consequences of these factors in host populations are difficult to study in natural settings. Much of our current knowledge comes from a limited number of virus groups and few ecological studies. Alternatively, progress has been made in the detection of new viruses and in probing the molecular basis of behavioural manipulation of hosts that might influence virus transmission. An expanding theoretical framework provides guidelines on the conditions under which particular transmission strategies might evolve, and their dynamical consequences, but empirical tests are lacking.
Detection of low levels of baculovirus for outbreak-terminating epizootics in defoliating insects
Recent empirical and theoretical studies have indicated that epizootics of baculoviruses in defoliating insects may result in the termination of outbreaks starting from lower initial infection rates than previously believed. This suggests that natural epizootics can preempt the need for costly and labor-intensive pest management measures because natural epizootics reduce or end outbreaks before substantial defoliation occurs. Such cases, however, require the ability to detect small amounts of infection at the beginning of the population's life cycle. At hatching, Douglas-fir tussock moth (Orgyia pseudotsugata) larvae become infected by baculoviruses on the surface of their eggs. Prior to the larval season in an outbreak area, egg masses are collected and assayed for the presence of viruses; however, a large number of eggs may need to be sampled to detect low infection rates in which biocontrol measures are not needed. Here we used simulated sampling to detect infection rates ranging from 10-3 to 10-4 and considered whether multiple potential probability distributions of the actual infection rate affected detection. We showed that the level of sampling is considerably higher than in previously published protocols, but that increased effort via either more egg masses sampled (with a fixed number of eggs per egg mass), or more eggs per egg mass sampled without collecting more egg masses, equally improved the accuracy of detecting the virus.