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Quantifying airborne dispersal routes of pathogens over continents to safeguard global wheat supply

Nature Plants volume 3, pages 780–786 (2017)Cite this article

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Abstract

Infectious crop diseases spreading over large agricultural areas pose a threat to food security. Aggressive strains of the obligate pathogenic fungus Puccinia graminis f.sp. tritici (Pgt), causing the crop disease wheat stem rust, have been detected in East Africa and the Middle East, where they lead to substantial economic losses and threaten livelihoods of farmers. The majority of commercially grown wheat cultivars worldwide are susceptible to these emerging strains, which pose a risk to global wheat production, because the fungal spores transmitting the disease can be wind-dispersed over regions and even continents1,2,3,4,5,6,7,8,9,10,11. Targeted surveillance and control requires knowledge about airborne dispersal of pathogens, but the complex nature of long-distance dispersal poses significant challenges for quantitative research12,13,14. We combine international field surveys, global meteorological data, a Lagrangian dispersion model and high-performance computational resources to simulate a set of disease outbreak scenarios, tracing billions of stochastic trajectories of fungal spores over dynamically changing host and environmental landscapes for more than a decade. This provides the first quantitative assessment of spore transmission frequencies and amounts amongst all wheat producing countries in Southern/East Africa, the Middle East and Central/South Asia. We identify zones of high air-borne connectivity that geographically correspond with previously postulated wheat rust epidemiological zones (characterized by endemic disease and free movement of inoculum)10,15, and regions with genetic similarities in related pathogen populations16,17. We quantify the circumstances (routes, timing, outbreak sizes) under which virulent pathogen strains such as ‘Ug99’5,6 pose a threat from long-distance dispersal out of East Africa to the large wheat producing areas in Pakistan and India. Long-term mean spore dispersal trends (predominant direction, frequencies, amounts) are summarized for all countries in the domain (Supplementary Data). Our mechanistic modelling framework can be applied to other geographic areas, adapted for other pathogens and used to provide risk assessments in real-time3.

The aim of the study described here was threefold: to develop a flexible data-driven simulation framework to analyse spore dispersal on regional and continental scales; to identify key airborne dispersal routes of Pgt-spores threatening wheat production; and to obtain estimates of typical airborne pathogen transmission quantities amongst donor and recipient countries to inform surveillance and control about risks when facing future outbreaks. We quantify when, how often and how many viable spores are dispersed from key disease locations to all susceptible and environmentally suitable wheat areas in Southern/East Africa, the Middle East and Central/South Asia. High-performance computing resources are used to link three dynamic data-driven modelling layers: landscapes of wheat fields, turbulent atmospheric dispersal of Pgt-urediniospores (hereafter also referred to as ‘spores’) and environmental suitability for infection after deposition (Methods and Supplementary Fig. 1). Based on global wheat production data18 and field surveys in more than 25 countries in Southern/East Africa, the Middle East and Central/South Asia over several years19, we identify a set of representative disease locations (RDLs; Supplementary Fig. 2) in countries, and determine those months of the year in which stem rust typically occurs in all countries of the geographical domain (Supplementary Video 1, Supplementary Fig. 3). From these RDLs during consecutive wheat seasons over 12 years (2003–2014), we simulate daily release, turbulent transport, loss of viability and deposition of Pgt-spores on susceptible and environmentally suitable wheat areas in receptor countries (Supplementary Videos 2 and 3). For the dispersal simulations we use NAME, the Lagrangian particle dispersion model (LPDM) of the UK Met Office20, adapted to biophysical characteristics of Pgt-urediniospores (as previously tested in a case-study of an epidemic in Ethiopia21) with a 3 day maximum lifetime during atmospheric transport. We determine if environmental conditions after dry and wet deposition are suitable for infection by developing an ecological niche model which we have tested against field disease survey data (Supplementary Videos 4 and 5, Supplementary Information Section 2.2). Both dispersal and environmental suitability calculations are driven by a three-dimensional grid of finely resolved (3-hourly; 17 km2 horizontal grid size; 59 vertical layers) global meteorological data from the UK Met Office’s Unified Model22.

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Fig. 1: Airborne dispersal routes of Pgt-spores causing wheat stem rust.
Fig. 2: Risk of atmospheric transmission of Pgt-spores to South Asia.
Fig. 3: The Rift Valley Pgt-spore incursion pathway.

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Acknowledgements

The authors are very grateful for financial support from the Bill & Melinda Gates Foundation, BBSRC, Friedrich-Ebert-Stiftung and DFID, UK. We thank all in-country field scientists who have contributed information on wheat cropping patterns and disease surveys. We acknowledge very useful discussion and support from members of the Epidemiology & Modelling Group in Cambridge.

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Authors and Affiliations

  1. Epidemiology and Modelling Group, Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK

    M. Meyer, J. A. Cox, M. D. T. Hitchings & C. A. Gilligan

  2. Atmospheric Dispersion and Air Quality (ADAQ), Met Office, Exeter, EX1 3PB, UK

    L. Burgin & M. C. Hort

  3. International Maize and Wheat Improvement Center (CIMMYT), PO Box 5689, Addis Ababa, Ethiopia

    D. P. Hodson

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Contributions

C.A.G. conceived the original project and modelling approach. M.M., J.A.C. and M.D.T.H. developed, tested and implemented the modelling framework, and performed the simulations and data-analysis in close collaboration with L.B. and M.C.H. and other members of the Epidemiology & Modelling Group in Cambridge. D.P.H. provided field survey data and wheat rust expertise and contacted international surveillance experts. M.M. wrote the manuscript and created the figures in collaboration with other authors. L.B., D.P.H. and C.A.G supervised the project.

Corresponding authors

Correspondence to M. Meyer or C. A. Gilligan.

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The authors declare no competing financial interests.

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Supplementary Information

Supplementary Figures 1–11; Supplementary Tables 1–4; Supplementary Methods; Supplementary Notes.

Life sciences reporting summary

Life sciences reporting summary

Supplementary Data 1

Seasonal Pgt spore dispersal trends from key wheat stem rust disease locations in Southern/East Africa, the Middle East and Central/South Asia.

Supplementary Data 2

Pgt spore dispersal frequencies and amounts amongst wheat producing countries in Southern/East Africa, the Middle East and Central/South Asia.

Supplementary Video 1

Main wheat stem rust seasons in countries in Southern/East Africa, the Middle East and Central/South Asia.

Supplementary Video 2

3D animation of atmospheric dispersal simulations of Pgt spores.

Supplementary Video 3

Time-lapse of daily Pgt spore deposition patterns resulting from daily simulation of spore release from the Bale Zone, Ethiopia, during the main wheat season of 2014.

Supplementary Video 4

Time-lapse of hourly meteorological surface fields (relative humidity) used to drive the environmental suitability calculations.

Supplementary Video 5

Time-lapse of the daily binary environmental suitability score obtained from the environmental suitability.

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Meyer, M., Cox, J.A., Hitchings, M.D.T. et al. Quantifying airborne dispersal routes of pathogens over continents to safeguard global wheat supply. Nature Plants 3, 780–786 (2017). https://doi.org/10.1038/s41477-017-0017-5

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