Probabilistic risk-based model for the assessment of Phyllosticta citricarpa-infected citrus fruit and illicit plant material as pathways for pathogen introduction and establishment

Authors: GOTTWALD, TIMOTHY - Retired ARS Employee; Taylor, Earl; AMORIM, L - University Of São Paulo; BERGAMIN-FILHO, A - University Of São Paulo; BASSANEZI, R - Fundecitrus - Brazil; SILVA JR., G - Fundecitrus - Brazil; FOGLIATA, G - Estacion Experimental Agroindustrial Obispo Colombres (EEAOC); FOURIE, P - University Of Stellenbosch; GRAHAM, JAMES - University Of Florida; HATTINGH, V - University Of Florida; KRISS, A - Syngenta Crop Production; LUO, W - North Carolina State University; MAGAREY, R - North Carolina State University; SCHUTTE, G - Citrus Research International (CRI); SPOSITO, M - University Of São Paulo

Submitted to: Crop Protection
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/18/2020
Publication Date: 12/22/2020
Citation: Gottwald, T.R., Taylor, E.L., Amorim, L., Bergamin-Filho, A., Bassanezi, R.B., Silva Jr., G.J., Fogliata, G., Fourie, P.H., Graham, J.H., Hattingh, V., Kriss, A.B., Luo, W., Magarey, R.D., Schutte, G.C., Sposito, M.B. 2020. Probabilistic risk-based model for the assessment of Phyllosticta citricarpa-infected citrus fruit and illicit plant material as pathways for pathogen introduction and establishment. Crop Protection. 142(2021) 105521. https://doi.org/10.1016/j.cropro.2020.105521.
DOI: https://doi.org/10.1016/j.cropro.2020.105521

Interpretive Summary: Citrus Black Spot (CBS) is a fungal disease of citrus. The pathogen causes lesions on fruit and plant material, alike, and is considered a quarantine pathogen in some countries. One concern expressed is that shipments of diseased fruit can lead to the spread of CBS into areas previously disease free. In this study, we examine ten (10) fruit trade pathways to quantify the risk of spreading CBS via fruit exports. In order to accomplish this task, we examined the environmental conditions at the point of production and export, and the final point of consumption for the importing country. The environmental conditions were required to determine if the fungus responsible for CBS could mature, disperse and lead to infection. Once we determined the probabilities of disease formation, spread and infection at each beginning and end-point, we examined current literature to identify and quantify mitigating factors of production and transport in areas were CBS is present to prevent and reduce the formation and spread of CBS. The reduction in disease and/or disease symptoms associated with these management practices were utilized to quantify the probability of disease spread within the selected trade routes. In addition to ascertaining the quantitative risk of exporting fruit and the spread of CBS, the authors also examined the potential for CBS spread by way of plant material. Whereas the risk of CBS spread via exporting fruit was minimal to negligible, the risk of disease introduction associated with plant material was significant.

Technical Abstract: Citrus Black Spot (CBS), caused by the ascomycete, Phyllosticta citricarpa is a fruit, foliar, and twig spotting fungal disease affecting the majority of commercial cultivars of citrus. The disease may cause fruit drop and cosmetic lesions, but P. citricarpa is considered a quarantine pathogen by some countries, impacting domestic and international trade of citrus fruit. Countries where P. citricarpa is considered a quarantine pathogen may require exporting countries where CBS occurs to implement one or more of the following measures: only export fruit from pest-free production areas, apply pre-harvest fungicide controls, exclude fruit through packinghouse grading, apply packinghouse treatments and conduct fruit inspection and shipping consignment rejection. These regulatory requirements exist even though there is no documented case of disease spread via infected fruit into previously disease-free areas. To clarify the risk of fruit as a potential pathway for the spread of CBS, we developed a quantitative, probabilistic-risk assessment model, i.e. tool. The model provides an assessment of all steps in the fruit pathway, including production, packinghouse handling, transportation, export-import distribution channels, and consumer endpoints. The model is stochastic and uses Monte Carlo simulation to assess the risk of P. citricarpa moving through all steps in the pathway. We attempted to use all available literature and information to quantitate risk at each point in the potential pathway and by sequentially linking all steps to determine the overall quantitative risk. In addition, we assessed climatological effects on incidence of diseased fruit at production sites and on fungal reproduction and infection as well as criteria for establishment at endpoints. We examined ten case studies between exporting and importing locations/countries. Model results indicated fruit to be an epidemiologically insignificant means for CBS spread, even between producing countries where CBS occurs and CBS-free importing countries with disease-conducive climates. We created a second model to examine the introduction of illicit plant material from countries where CBS occurs. This model demonstrated significant probability of introduction via such illicit material, identifying a probable pathway. However, the second model demonstrated that even though spread was likely via plant material, pathogen establishment and disease development was still restricted only to areas with conducive climatological conditions. We created a tool to quantitatively explore the viability of various potential pathways via combinations of CBS-present production sites and corresponding pathway endpoints, including environments conducive and non-conducive to CBS. The tool is provided to aid decision makers on phytosanitary risk relative to international trade of citrus fruit.