Inoculum dose, diversity, dispersal, and damage: Simulating optimal economic control of hop powdery mildew at the landscape level

Abstract

CONTEXT Plant pathogens that disperse by airborne propagules may cause damage that extends beyond the borders of individual fields. Developing sound management strategies, therefore, requires consideration of heterogeneity in pathogen transmission, the effectiveness of control measures, host susceptibility and pathogen virulence, and the resulting economic outcomes that scale up at the regional level with coordinated management. OBJECTIVE We use hop powdery mildew as a motivating pathosystem to develop a coupled epidemiological-economic model to enable simulation of the impact of epidemic conditions and coordinated management interventions on profitability. This pathosystem is a well-suited case study because disease development may be limited by primary inoculum and fungicide applications, yet the pathogen can spread via long-distance dispersal between fields and rapidly damage both crop yield and quality. METHODS We parameterized the model using data collected from a census survey of commercial hop yards in Oregon during 2014 to 2017, including the monthly incidence of plants with powdery mildew, fungicides applied by growers, and estimated revenue depending on how the incidence of diseased hop cones affects yield and the likelihood of crop devaluation. We show that conditions in the early stages of epidemics related to primary inoculum dose, pathogen diversity, and the intensity of management intervention interact and determine the optimal regional control strategy. RESULTS AND CONCLUSIONS As the likelihood of primary infection increases, due to either the dose of primary inoculum or virulence of the pathogen population, mean profitability decreases. These effects are most pronounced when primary infection occurs in yards that are highly connected in the disease transmission network. The choice of how many fungicide applications to make in response to initial infection has little effect on profitability when the primary inoculum is relatively infrequent. However, as primary inoculum increases, targeted fungicide applications made in the early stages of epidemics are essential for maximizing profitability region-wide. These principles hold across a range of market demand scenarios that impose different crop quality standards, with the optimal number of early-season fungicide applications remaining largely consistent despite substantially different crop prices. SIGNIFICANCE Our analysis addresses a multifaceted challenge in agricultural disease management where epidemic control decisions must account for interactions between pathogen biology, management practices, market conditions, and regional-scale disease transmission. This research provides a framework for formally understanding factors that influence the cost of disease in complex systems where pathogens disperse across management units.