Eco-Epidemiological Uncertainties of Emerging Plant Diseases: The Challenge of Predicting Xylella fastidiosa Dynamics in Novel Environments

In order to prevent and control the emergence of biosecurity threats such as vector-borne diseases of plants, it is vital to understand drivers of entry, establishment, and spatiotemporal spread, as well as the form, timing, and effectiveness of disease management strategies. An inherent challenge for policy in combatting emerging disease is the uncertainty associated with intervention planning in areas not yet affected, based on models and data from current outbreaks. Following the recent high-profile emergence of the bacterium Xylella fastidiosa in a number of European countries, we review the most pertinent epidemiological uncertainties concerning the dynamics of this bacterium in novel environments. To reduce the considerable ecological and socio-economic impacts of these outbreaks, eco-epidemiological research in a broader range of environmental conditions needs to be conducted and used to inform policy to enhance disease risk assessment, and support successful policy-making decisions. By characterizing infection pathways, we can highlight the uncertainties that surround our knowledge of this disease, drawing attention to how these are amplified when trying to predict and manage outbreaks in currently unaffected locations. To help guide future research and decision-making processes, we invited experts in different fields of plant pathology to identify data to prioritize when developing pest risk assessments. Our analysis revealed that epidemiological uncertainty is mainly driven by the large variety of hosts, vectors, and bacterial strains, leading to a range of different epidemiological characteristics further magnified by novel environmental conditions. These results offer new insights on how eco-epidemiological analyses can enhance understanding of plant disease spread and support management recommendations. [Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY 4.0 International license .

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Impact of Xylella fastidiosa subspecies pauca in European olives

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1912206117 ◽

2020 ◽

Vol 117 (17) ◽

pp. 9250-9259 ◽

Cited By ~ 17

Author(s):

Kevin Schneider ◽

Wopke van der Werf ◽

Martina Cendoya ◽

Monique Mourits ◽

Juan A. Navas-Cortés ◽

...

Keyword(s):

Xylella Fastidiosa ◽

Plant Diseases ◽

Disease Spread ◽

Economic Damage ◽

Climatic Suitability ◽

Case Scenario ◽

Worst Case ◽

Ongoing Research ◽

Phytosanitary Measures ◽

The Impact

Xylella fastidiosa is the causal agent of plant diseases that cause massive economic damage. In 2013, a strain of the bacterium was, for the first time, detected in the European territory (Italy), causing the Olive Quick Decline Syndrome. We simulate future spread of the disease based on climatic-suitability modeling and radial expansion of the invaded territory. An economic model is developed to compute impact based on discounted foregone profits and losses in investment. The model projects impact for Italy, Greece, and Spain, as these countries account for around 95% of the European olive oil production. Climatic suitability modeling indicates that, depending on the suitability threshold, 95.5 to 98.9%, 99.2 to 99.8%, and 84.6 to 99.1% of the national areas of production fall into suitable territory in Italy, Greece, and Spain, respectively. For Italy, across the considered rates of radial range expansion the potential economic impact over 50 y ranges from 1.9 billion to 5.2 billion Euros for the economic worst-case scenario, in which production ceases after orchards die off. If replanting with resistant varieties is feasible, the impact ranges from 0.6 billion to 1.6 billion Euros. Depending on whether replanting is feasible, between 0.5 billion and 1.3 billion Euros can be saved over the course of 50 y if disease spread is reduced from 5.18 to 1.1 km per year. The analysis stresses the necessity to strengthen the ongoing research on cultivar resistance traits and application of phytosanitary measures, including vector control and inoculum suppression, by removing host plants.

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Improving Management Strategies of Plant Diseases Using Sequential Sensitivity Analyses

Phytopathology ◽

10.1094/phyto-06-18-0196-r ◽

2019 ◽

Vol 109 (7) ◽

pp. 1184-1197 ◽

Cited By ~ 7

Author(s):

Loup Rimbaud ◽

Sylvie Dallot ◽

Claude Bruchou ◽

Sophie Thoyer ◽

Emmanuel Jacquot ◽

...

Keyword(s):

Net Present Value ◽

Management Strategies ◽

Optimal Solution ◽

Plant Diseases ◽

Control Measures ◽

Disease Suppression ◽

Simultaneous Optimization ◽

Disease Spread ◽

Sensitivity Analyses ◽

Plum Pox Virus

Improvement of management strategies of epidemics is often hampered by constraints on experiments at large spatiotemporal scales. A promising approach consists of modeling the biological epidemic process and human interventions, which both impact disease spread. However, few methods enable the simultaneous optimization of the numerous parameters of sophisticated control strategies. To do so, we propose a heuristic approach (i.e., a practical improvement method approximating an optimal solution) based on sequential sensitivity analyses. In addition, we use an economic improvement criterion based on the net present value, accounting for both the cost of the different control measures and the benefit generated by disease suppression. This work is motivated by sharka (caused by Plum pox virus), a vector-borne disease of prunus trees (especially apricot, peach, and plum), the management of which in orchards is mainly based on surveillance and tree removal. We identified the key parameters of a spatiotemporal model simulating sharka spread and control and approximated optimal values for these parameters. The results indicate that the current French management of sharka efficiently controls the disease, but it can be economically improved using alternative strategies that are identified and discussed. The general approach should help policy makers to design sustainable and cost-effective strategies for disease management.

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Mathematical models are a powerful method to understand and control the spread of Huanglongbing

10.7287/peerj.preprints.2059 ◽

2016 ◽

Author(s):

Rachel A Taylor ◽

Erin Mordecai ◽

Christopher A Gilligan ◽

Jason R Rohr ◽

Leah R Johnson

Keyword(s):

Data Collection ◽

Mathematical Models ◽

Management Strategies ◽

Intervention Strategy ◽

Cost Effective ◽

Plant Diseases ◽

Disease Spread ◽

Vector Borne ◽

Almost All ◽

And Control

Huanglongbing, or citrus greening, is a global citrus disease occurring in almost all citrus growing regions and causing substantial economic burdens to individual growers, citrus industries and governments. Successful management strategies to reduce disease burden are desperately needed but with so many possible interventions and combinations thereof, it is difficult to know which are worthwhile or cost-effective. We review how mathematical models have yielded useful insights into controlling disease spread for other vector-borne plant diseases, and the small number of mathematical models of Huanglongbing. We adapt a malaria model to Huanglongbing, by including temperature-dependent psyllid traits and economic costs, to show how models can be used to highlight which parameters require more data collection or which should be targeted for intervention. We analyze the most common intervention strategy, insecticide spraying, to determine the most cost-effective spraying strategy. We found that fecundity and feeding rate of the vector require more experimental data collection, for wider temperatures ranges. The best strategy for insecticide intervention was to spray for more days rather than pay extra for a more efficient spray. We conclude that mathematical models are able to provide useful recommendations for managing Huanglongbing spread.

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Improving management strategies of plant diseases using sequential sensitivity analyses

10.1101/315747 ◽

2018 ◽

Author(s):

Loup Rimbaud ◽

Sylvie Dallot ◽

Claude Bruchou ◽

Sophie Thoyer ◽

Emmanuel Jacquot ◽

...

Keyword(s):

Net Present Value ◽

Control Strategies ◽

Management Strategies ◽

Optimal Solution ◽

Plant Diseases ◽

Control Measures ◽

Disease Suppression ◽

Disease Spread ◽

Sensitivity Analyses ◽

Plum Pox Virus

ABSTRACTImprovement of management strategies of epidemics is often hampered by constraints on experiments at large spatiotemporal scales. A promising approach consists of modelling the biological epidemic process and human interventions, which both impact disease spread. However, few methods enable the simultaneous optimisation of the numerous parameters of sophisticated control strategies. To do so, we propose a heuristic approach (i.e., a practical improvement method approximating an optimal solution) based on sequential sensitivity analyses. In addition, we use an economic improvement criterion, based on the net present value, accounting for both the cost of the different control measures and the benefit generated by disease suppression. This work is motivated by sharka (caused by Plum pox virus), a vector-borne disease of prunus trees (especially apricot, peach and plum) whose management in orchards is mainly based on surveillance and tree removal. We identified the key parameters of a spatiotemporal model simulating sharka spread and control, and approximated optimal values for these parameters. The results indicate that the current French management of sharka efficiently controls the disease, but can be economically improved using alternative strategies that are identified and discussed. The general approach should help policymakers to design sustainable and cost-effective strategies for disease management.

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Microbial Biocontrol Strategies for Ambrosia Beetles and Their Associated Phytopathogenic Fungi

Frontiers in Sustainable Food Systems ◽

10.3389/fsufs.2021.737977 ◽

2021 ◽

Vol 5 ◽

Author(s):

Frédérique Reverchon ◽

Silvia M. Contreras-Ramos ◽

Akif Eskalen ◽

José A. Guerrero-Analco ◽

Evangelina E. Quiñones-Aguilar ◽

...

Keyword(s):

Natural Products ◽

Antifungal Activity ◽

Management Strategies ◽

Biocontrol Agents ◽

Future Research ◽

Bacterial Strains ◽

Ambrosia Beetles ◽

Positive Effects ◽

Microbial Natural Products

Ambrosia beetles and their symbiotic fungi are causing severe damage in natural and agro-ecosystems worldwide, threatening the productivity of several important tree crops such as avocado. Strategies aiming at mitigating their impact include the application of broad-spectrum agrochemicals and the incineration of diseased trees, but the increasing demand for environment-friendly strategies call for exploring biological control for the management of ambrosia beetles and their phytopathogenic fungal symbionts. The aim of this review is to examine the existing knowledge on biocontrol approaches using beneficial microorganisms and microbial natural products with entomopathogenic and antifungal activity against ambrosia beetles and fungi. We show that biocontrol has been mainly focused on the insect, using entomopathogenic fungi (EPF) such as Beauveria spp. or Metarhizium spp. However, recent studies have been integrating EPF with mycoparasitic fungi such as Trichoderma spp. to simultaneously challenge the vector and its fungal symbionts. Novel approaches also include the use of microbial natural products as insect lures or antifungal agents. Contrastingly, the potential of bacteria, including actinobacteria (actinomycetes), as biocontrol agents of ambrosia fungi has been little investigated. We thus suggest that future research should further examine the antifungal activity of bacterial strains, with an emphasis on harsh environments. We also suggest pursuing the isolation of more effective microbial strains with dual biocontrol effect, i.e., exhibiting fungicidal/insecticidal activities. Moreover, additional efforts should aim at determining the best application methods of biocontrol agents in the field to ensure that the positive effects detected in vitro are sustained. Finally, we propose the integration of microbiome studies in pest and disease management strategies as they could provide us with tools to steer the beneficial host plant microbiome and to manipulate the beetle microbiome in order to reduce insect fitness.

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From Nucleotides to Satellite Imagery: Approaches to Identify and Manage the Invasive Pathogen Xylella fastidiosa and Its Insect Vectors in Europe

Sustainability ◽

10.3390/su12114508 ◽

2020 ◽

Vol 12 (11) ◽

pp. 4508 ◽

Cited By ~ 5

Author(s):

Francesca Raffini ◽

Giorgio Bertorelle ◽

Roberto Biello ◽

Guido D’Urso ◽

Danilo Russo ◽

...

Keyword(s):

Invasive Species ◽

Spatial Ecology ◽

Xylella Fastidiosa ◽

Plant Diseases ◽

Future Research ◽

Insect Vectors ◽

Research Directions ◽

Future Research Directions ◽

Vector Borne ◽

European Agriculture

Biological invasions represent some of the most severe threats to local communities and ecosystems. Among invasive species, the vector-borne pathogen Xylella fastidiosa is responsible for a wide variety of plant diseases and has profound environmental, social and economic impacts. Once restricted to the Americas, it has recently invaded Europe, where multiple dramatic outbreaks have highlighted critical challenges for its management. Here, we review the most recent advances on the identification, distribution and management of X. fastidiosa and its insect vectors in Europe through genetic and spatial ecology methodologies. We underline the most important theoretical and technological gaps that remain to be bridged. Challenges and future research directions are discussed in the light of improving our understanding of this invasive species, its vectors and host–pathogen interactions. We highlight the need of including different, complimentary outlooks in integrated frameworks to substantially improve our knowledge on invasive processes and optimize resources allocation. We provide an overview of genetic, spatial ecology and integrated approaches that will aid successful and sustainable management of one of the most dangerous threats to European agriculture and ecosystems.

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Environment-Pathogen Interaction in Plant Diseases

Agricultural Reviews ◽

10.18805/ag.r-1859 ◽

2019 ◽

Vol 40 (03) ◽

Author(s):

Rajat Sharma ◽

Shalini Verma

Keyword(s):

Carbon Dioxide ◽

Environmental Conditions ◽

Management Strategies ◽

Global Environmental Change ◽

Carbon Dioxide Concentration ◽

Plant Ecology ◽

Plant Diseases ◽

Elevated Concentration ◽

Natural Ecosystem ◽

Environment Change

nvironment is an important aspect of plant ecology and global environmental change is of major concern that is caused by natural and human activities which alter greenhouse gas concentrations in the atmosphere. The increase in concentration of greenhouse gases is foreseen to continue to raise average global temperature. Elevated concentration of carbon dioxide with increased temperature influences the plant-disease interactions. The environment has an influence over the development as well as temporal and spatial dissemination of plant diseases. The result of change in environment can either be favorable, non favorable or impartial, as these changes can either lessen, expand or have no influence on diseases as each disease may be attributed differently to these variations in accordance to an area or time of year. Variation in environmental conditions is said to be influencing plants in natural ecosystems all around the world and change in climate directly impacts crops, along with their synergy in accordance with the microbial population. The important elements governing magnification and spread of plant diseases are temperature, moisture, light and carbon dioxide concentration. Environment change causes a significant impact on germination, reproduction, sporulation, spore dispersal, along with perforation by pathogens as a vulnerable host will not be invaded by a pernicious pathogen if the environmental conditions are not facilitative for disease. The environment influences all life stages of host as well as that of a pathogen and as a result induces an opposition to various pathosystems. Resistance mechanisms of plants, including effector-triggered immunity (ETI), pattern-triggered immunity (PTI) and defence network of hormones, are particularly influenced by environmental elements. Pathogenic virulence mechanisms like fabrication of virulence proteins and toxins, and also spore germination and survival are governed by factors such as atmospheric carbon dioxide, temperature and humidity. A large number of in-vitro experiments to understand interactions between plants and pathogens rely on predetermined pathosystems by making use of ascertained environmental conditions which take into consideration relatively small part of vital plant–pathogen–environment interactions occurring in natural ecosystem. Thus, there is a need to research effectiveness of disease management strategies that is, to assess current management strategies to understand multifaceted nature of environment-pathogen interactions for production of crops that are irrepressible to environment change.

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Mathematical models are a powerful method to understand and control the spread of Huanglongbing

PeerJ ◽

10.7717/peerj.2642 ◽

2016 ◽

Vol 4 ◽

pp. e2642 ◽

Cited By ~ 24

Author(s):

Rachel A. Taylor ◽

Erin A. Mordecai ◽

Christopher A. Gilligan ◽

Jason R. Rohr ◽

Leah R. Johnson

Keyword(s):

Data Collection ◽

Mathematical Models ◽

Management Strategies ◽

Intervention Strategy ◽

Cost Effective ◽

Plant Diseases ◽

Disease Spread ◽

Vector Borne ◽

Almost All ◽

And Control

Huanglongbing (HLB), or citrus greening, is a global citrus disease occurring in almost all citrus growing regions. It causes substantial economic burdens to individual growers, citrus industries and governments. Successful management strategies to reduce disease burden are desperately needed but with so many possible interventions and combinations thereof it is difficult to know which are worthwhile or cost-effective. We review how mathematical models have yielded useful insights into controlling disease spread for other vector-borne plant diseases, and the small number of mathematical models of HLB. We adapt a malaria model to HLB, by including temperature-dependent psyllid traits, “flushing” of trees, and economic costs, to show how models can be used to highlight the parameters that require more data collection or that should be targeted for intervention. We analyze the most common intervention strategy, insecticide spraying, to determine the most cost-effective spraying strategy. We find that fecundity and feeding rate of the vector require more experimental data collection, for wider temperatures ranges. Also, the best strategy for insecticide intervention is to spray for more days rather than pay extra for a more efficient spray. We conclude that mathematical models are able to provide useful recommendations for managing HLB spread.

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Integrating natural and social science perspectives on plant disease risk, management and policy formulation

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2010.0411 ◽

2011 ◽

Vol 366 (1573) ◽

pp. 2035-2044 ◽

Cited By ~ 47

Author(s):

Peter Mills ◽

Katharina Dehnen-Schmutz ◽

Brian Ilbery ◽

Mike Jeger ◽

Glyn Jones ◽

...

Keyword(s):

Risk Management ◽

Pathogen Detection ◽

Plant Disease ◽

Disease Risk ◽

Research Effort ◽

Management Strategies ◽

Policy Formulation ◽

Plant Diseases ◽

Natural Environments ◽

Natural Ecosystems

Plant diseases threaten both food security and the botanical diversity of natural ecosystems. Substantial research effort is focused on pathogen detection and control, with detailed risk management available for many plant diseases. Risk can be assessed using analytical techniques that account for disease pressure both spatially and temporally. We suggest that such technical assessments of disease risk may not provide an adequate guide to the strategies undertaken by growers and government to manage plant disease. Instead, risk-management strategies need to account more fully for intuitive and normative responses that act to balance conflicting interests between stakeholder organizations concerned with plant diseases within the managed and natural environments. Modes of effective engagement between policy makers and stakeholders are explored in the paper, together with an assessment of such engagement in two case studies of contemporary non-indigenous diseases in one food and in one non-food sector. Finally, a model is proposed for greater integration of stakeholders in policy decisions.

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The Impact of Climate Change on Agricultural Insect Pests

Insects ◽

10.3390/insects12050440 ◽

2021 ◽

Vol 12 (5) ◽

pp. 440

Author(s):

Sandra Skendžić ◽

Monika Zovko ◽

Ivana Pajač Živković ◽

Vinko Lešić ◽

Darija Lemić

Keyword(s):

Climate Change ◽

Insect Pests ◽

Management Strategies ◽

Interspecific Interaction ◽

Plant Diseases ◽

Economic Losses ◽

Future Research ◽

Pest Population ◽

Increased Risk ◽

The Impact

Climate change and global warming are of great concern to agriculture worldwide and are among the most discussed issues in today’s society. Climate parameters such as increased temperatures, rising atmospheric CO2 levels, and changing precipitation patterns have significant impacts on agricultural production and on agricultural insect pests. Changes in climate can affect insect pests in several ways. They can result in an expansion of their geographic distribution, increased survival during overwintering, increased number of generations, altered synchrony between plants and pests, altered interspecific interaction, increased risk of invasion by migratory pests, increased incidence of insect-transmitted plant diseases, and reduced effectiveness of biological control, especially natural enemies. As a result, there is a serious risk of crop economic losses, as well as a challenge to human food security. As a major driver of pest population dynamics, climate change will require adaptive management strategies to deal with the changing status of pests. Several priorities can be identified for future research on the effects of climatic changes on agricultural insect pests. These include modified integrated pest management tactics, monitoring climate and pest populations, and the use of modelling prediction tools.

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