Optimal strategies to protect a sub-population at risk due to an established epidemic.

Epidemics can particularly threaten certain sub-populations. For example, for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the elderly are often preferentially protected. For diseases of plants and animals, certain sub-populations can drive mitigation because they are intrinsically more valuable for ecological, economic, socio-cultural or political reasons. Here, we use optimal control theory to identify strategies to optimally protect a 'high-value' sub-population when there is a limited budget and epidemiological uncertainty. We use protection of the Redwood National Park in California in the face of the large ongoing state-wide epidemic of sudden oak death (caused by Phytophthora ramorum) as a case study. We concentrate on whether control should be focused entirely within the National Park itself, or whether treatment of the growing epidemic in the surrounding 'buffer region' can instead be more profitable. We find that, depending on rates of infection and the size of the ongoing epidemic, focusing control on the high-value region is often optimal. However, priority should sometimes switch from the buffer region to the high-value region only as the local outbreak grows. We characterize how the timing of any switch depends on epidemiological and logistic parameters, and test robustness to systematic misspecification of these factors due to imperfect prior knowledge

Optimising reactive disease management using spatially explicit models at the landscape scale

Increasing rates of global trade and travel, as well as changing climatic patterns, have led to more frequent outbreaks of plant disease epidemics worldwide. Mathematical modelling is a key tool in predicting where and how these new threats will spread, as well as in assessing how damaging they might be. Models can also be used to inform disease management, providing a rational methodology for comparing the performance of possible control strategies against one another. For emerging epidemics, in which new pathogens or pathogen strains are actively spreading into new regions, the spatial component of spread becomes particularly important, both to make predictions and to optimise disease control. In this chapter we illustrate how the spatial spread of emerging plant diseases can be modelled at the landscape scale via spatially explicit compartmental models. Our particular focus is on the crucial role of the dispersal kernel-which parameterises the probability of pathogen spread from an infected host to susceptible hosts at any given distance-in determining outcomes of epidemics. We add disease management to our model by testing performance of a simple "one off" form of reactive disease control, in which sites within a particular distance of locations detected to contain infection are removed in a single round of disease management. We use this simplified model to show how ostensibly arcane decisions made by the modeller-most notably whether or not the underpinning disease model allows for stochasticity (i.e. randomness)-can greatly impact on disease management recommendations. Our chapter is accompanied by example code in the programming language R available via an online repository, allowing the reader to run the models we present for him/herself

An ecophysiological model of plant-pest interactions: the role of nutrient and water availability.

Empirical studies have shown that particular irrigation/fertilization regimes can reduce pest populations in agroecosystems. This appears to promise that the ecological concept of bottom-up control can be applied to pest management. However, a conceptual framework is necessary to develop a mechanistic basis for empirical evidence. Here, we couple a mechanistic plant growth model with a pest population model. We demonstrate its utility by applying it to the peach-green aphid system. Aphids are herbivores which feed on the plant phloem, deplete plants' resources and (potentially) transmit viral diseases. The model reproduces system properties observed in field studies and shows under which conditions the diametrically opposed plant vigour and plant stress hypotheses find support. We show that the effect of fertilization/irrigation on the pest population cannot be simply reduced as positive or negative. In fact, the magnitude and direction of any effect depend on the precise level of fertilization/irrigation and on the date of observation. We show that a new synthesis of experimental data can emerge by embedding a mechanistic plant growth model, widely studied in agronomy, in a consumer-resource modelling framework, widely studied in ecology. The future challenge is to use this insight to inform practical decision making by farmers and growers

Pathogenic modification of plants enhances long-distance dispersal of non-persistently transmitted viruses to new hosts.

Aphids spread the majority of plant viruses through ‘non-persistent’ transmission (NPT) whereby virus particles attach transiently to these insects’ probing mouthparts. Virus acquisition from infected plants and inoculation to healthy host plants is favored when aphids briefly probe plant epidermal cells. It is well established that NPT virus infection can alter plant-vector interactions, and moreover such pathogen modifications are found in a range of plant and animal systems. In particular, viruses can make plants more attractive to aphids but inhibit aphid settling on infected plants. It is hypothesized that this viral ‘reprogramming’ of plants promotes virus acquisition and encourages dispersal of virus-bearing aphids to fresh hosts. In contrast, it is hypothesized that virus-induced biochemical changes encouraging prolonged feeding on infected hosts inhibit NPT. To understand how these virus-induced modifications affect epidemics, we developed a modeling framework accounting for important but often neglected factors, including: feeding behaviors (probing or prolonged feeding) and distinct spatial scales of transmission (as conditioned by wingless or winged aphids). Analysis of our models confirmed that when viruses inhibit aphid settling on infected plants this initially promotes virus transmission. However, initially enhanced transmission is self-limiting because it decreases vector density. Another important finding is that virus-induced changes encouraging settling will stimulate birth of winged aphids, which promotes epidemics of NPT viruses over greater distances. Thus our results illustrate how plant virus modifications influence epidemics by altering vector distribution, density, and even vector form. Our insights are important for understanding how pathogens in general propagate through natural plant communities and crops

Detecting Presymptomatic Infection Is Necessary to Forecast Major Epidemics in the Earliest Stages of Infectious Disease Outbreaks.

We assess how presymptomatic infection affects predictability of infectious disease epidemics. We focus on whether or not a major outbreak (i.e. an epidemic that will go on to infect a large number of individuals) can be predicted reliably soon after initial cases of disease have appeared within a population. For emerging epidemics, significant time and effort is spent recording symptomatic cases. Scientific attention has often focused on improving statistical methodologies to estimate disease transmission parameters from these data. Here we show that, even if symptomatic cases are recorded perfectly, and disease spread parameters are estimated exactly, it is impossible to estimate the probability of a major outbreak without ambiguity. Our results therefore provide an upper bound on the accuracy of forecasts of major outbreaks that are constructed using data on symptomatic cases alone. Accurate prediction of whether or not an epidemic will occur requires records of symptomatic individuals to be supplemented with data concerning the true infection status of apparently uninfected individuals. To forecast likely future behavior in the earliest stages of an emerging outbreak, it is therefore vital to develop and deploy accurate diagnostic tests that can determine whether asymptomatic individuals are actually uninfected, or instead are infected but just do not yet show detectable symptoms.This is the final version of the article. It first appeared from PLOS via http://dx.doi.org/10.1371/journal.pcbi.100483

When Does Spatial Diversification Usefully Maximize the Durability of Crop Disease Resistance?

Maximizing the durability of crop disease resistance genes in the face of pathogen evolution is a major challenge in modern agricultural epidemiology. Spatial diversification in the deployment of resistance genes, where susceptible and resistant fields are more closely intermixed, is predicted to drive lower epidemic intensities over evolutionary timescales. This is due to an increase in the strength of dilution effects, caused by pathogen inoculum challenging host tissue to which it is not well-specialized. The factors that interact with and determine the magnitude of this spatial suppressive effect are not currently well understood, however, leading to uncertainty over the pathosystems where such a strategy is most likely to be cost-effective. We model the effect on landscape scale disease dynamics of spatial heterogeneity in the arrangement of fields planted with either susceptible or resistant cultivars, and the way in which this effect depends on the parameters governing the pathosystem of interest. Our multiseason semidiscrete epidemiological model tracks spatial spread of wild-type and resistance-breaking pathogen strains, and incorporates a localized reservoir of inoculum, as well as the effects of within and between field transmission. The pathogen dispersal characteristics, any fitness cost(s) of the resistance-breaking trait, the efficacy of host resistance, and the length of the timeframe of interest all influence the strength of the spatial diversification effect. A key result is that spatial diversification has the strongest beneficial effect at intermediate fitness costs of the resistance-breaking trait, an effect driven by a complex set of nonlinear interactions. On the other hand, however, if the resistance-breaking strain is not fit enough to invade the landscape, then a partially effective resistance gene can result in spatial diversification actually worsening the epidemic. These results allow us to make general predictions of the types of system for which spatial diversification is most likely to be cost-effective, paving the way for potential economic modeling and pathosystem specific evaluation. These results highlight the importance of studying the effect of genetics on landscape scale spatial dynamics within host-pathogen disease systems.[Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY 4.0 International license

Epidemiological and ecological consequences of virus manipulation of host and vector in plant virus transmission.

Many plant viruses are transmitted by insect vectors. Transmission can be described as persistent or non-persistent depending on rates of acquisition, retention, and inoculation of virus. Much experimental evidence has accumulated indicating vectors can prefer to settle and/or feed on infected versus noninfected host plants. For persistent transmission, vector preference can also be conditional, depending on the vector's own infection status. Since viruses can alter host plant quality as a resource for feeding, infection potentially also affects vector population dynamics. Here we use mathematical modelling to develop a theoretical framework addressing the effects of vector preferences for landing, settling and feeding-as well as potential effects of infection on vector population density-on plant virus epidemics. We explore the consequences of preferences that depend on the host (infected or healthy) and vector (viruliferous or nonviruliferous) phenotypes, and how this is affected by the form of transmission, persistent or non-persistent. We show how different components of vector preference have characteristic effects on both the basic reproduction number and the final incidence of disease. We also show how vector preference can induce bistability, in which the virus is able to persist even when it cannot invade from very low densities. Feedbacks between plant infection status, vector population dynamics and virus transmission potentially lead to very complex dynamics, including sustained oscillations. Our work is supported by an interactive interface https://plantdiseasevectorpreference.herokuapp.com/. Our model reiterates the importance of coupling virus infection to vector behaviour, life history and population dynamics to fully understand plant virus epidemics

Can rainfall be a useful predictor of epidemic risk across temporal and spatial scales?

Plant disease epidemics are largely driven by within-season weather variables when inoculum is not limiting. Commonly, predictors in risk assessment models are based on the interaction of temperature and wetness-related variables, relationships which are determined experimentally. There is an increasing interest in providing within-season or inter-seasonal risk information at the region or continent scale, which commonly use models developed for a smaller scale. Hence, the scale matching dilemma that challenges epidemiologists and meteorologists: upscale models or downscale weather data? Successful applications may be found in both cases, which should be supported by validation datasets whenever possible, to prove the usefulness of the approach. For some diseases, rainfall is key for inoculum dispersal and, in warmer regions (e.g., tropics) where temperature is less limiting for epidemics, rainfall extends wetness periods. The drawbacks of using rainfall at small scales relate to its discrete nature and high spatial variability. However, for pre- or early-season predictions at large spatial scales sources of reasonably accurate rainfall summaries are available and may prove useful. The availability of disease datasets at various scales allows the development and evaluation of new models to be applied at the correct scale. We will showcase examples and discuss the usefulness of rainfall as key variable to predict soybean rust and wheat scab from field to region