Potential distribution of Biscogniauxia mediterranea and Obolarina persica causal agents of oak charcoal disease in Iran’s Zagros forests

Abstract In Iran, native oak species are under threat from episodes of Charcoal Disease, a decline syndrome driven by abiotic stressors (e.g. drought, elevated temperature) and biotic components, Biscogniauxia mediterranea (De Not.) Kuntze and Obolarina persica (M. Mirabolfathy). The outbreak is sti...

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Main Authors: Meysam BakhshiGanje, Shirin Mahmoodi, Kourosh Ahmadi, Mansoureh Mirabolfathy
Format: Article
Language:English
Published: Nature Portfolio 2024-04-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-024-57298-2
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author Meysam BakhshiGanje
Shirin Mahmoodi
Kourosh Ahmadi
Mansoureh Mirabolfathy
author_facet Meysam BakhshiGanje
Shirin Mahmoodi
Kourosh Ahmadi
Mansoureh Mirabolfathy
author_sort Meysam BakhshiGanje
collection DOAJ
description Abstract In Iran, native oak species are under threat from episodes of Charcoal Disease, a decline syndrome driven by abiotic stressors (e.g. drought, elevated temperature) and biotic components, Biscogniauxia mediterranea (De Not.) Kuntze and Obolarina persica (M. Mirabolfathy). The outbreak is still ongoing and the country’s largest ever recorded. Still, the factors driving its’ epidemiology in time and space are poorly known and such knowledge is urgently needed to develop strategies to counteract the adverse effects. In this study, we developed a generic framework based on experimental, machine-learning algorithms and spatial analyses for landscape-level prediction of oak charcoal disease outbreaks. Extensive field surveys were conducted during 2013–2015 in eight provinces (more than 50 unique counties) in the Zagros ecoregion. Pathogenic fungi were isolated and characterized through morphological and molecular approaches, and their pathogenicity was assessed under controlled water stress regimes in the greenhouse. Further, we evaluated a set of 29 bioclimatic, environmental, and host layers in modeling for disease incidence data using four well-known machine learning algorithms including the Generalized Linear Model, Gradient Boosting Model, Random Forest model (RF), and Multivariate Adaptive Regression Splines implemented in MaxEnt software. Model validation statistics [Area Under the Curve (AUC), True Skill Statistics (TSS)], and Kappa index were used to evaluate the accuracy of each model. Models with a TSS above 0.65 were used to prepare an ensemble model. The results showed that among the different climate variables, precipitation and temperature (Bio18, Bio7, Bio8, and bio9) in the case of O. persica and similarly, gsl (growing season length TREELIM, highlighting the warming climate and the endophytic/pathogenic nature of the fungus) and precipitation in case of B. mediterranea are the most important influencing variables in disease modeling, while near-surface wind speed (sfcwind) is the least important variant. The RF algorithm generates the most robust predictions (ROC of 0.95; TSS of 0.77 and 0.79 for MP and OP, respectively). Theoretical analysis shows that the ensemble model (ROC of 0.95 and 0.96; TSS = 0.79 and 0.81 for MP and OP, respectively), can efficiently be used in the prediction of the charcoal disease spatiotemporal distribution. The oak mortality varied ranging from 2 to 14%. Wood-boring beetles association with diseased trees was determined at 20%. Results showed that water deficiency is a crucial component of the oak decline phenomenon in Iran. The Northern Zagros forests (Ilam, Lorestan, and Kermanshah provinces) along with the southern Zagros forests (Fars and Kohgilouyeh va-Boyer Ahmad provinces) among others are the most endangered areas of potential future pandemics of charcoal disease. Our findings will significantly improve our understanding of the current situation of the disease to pave the way against pathogenic agents in Iran.
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spelling doaj.art-310e7e4c8c8a4e93881124d3ba52c5c52024-04-07T11:15:26ZengNature PortfolioScientific Reports2045-23222024-04-0114111410.1038/s41598-024-57298-2Potential distribution of Biscogniauxia mediterranea and Obolarina persica causal agents of oak charcoal disease in Iran’s Zagros forestsMeysam BakhshiGanje0Shirin Mahmoodi1Kourosh Ahmadi2Mansoureh Mirabolfathy3Kohgiluyeh va Boyer-Ahmad Agricultural and Natural Resources Research and Education CenterNational center of genetic resources, Agricultural Research Education and Extention OrganizationDepartment of Forestry, Faculty of Natural Resources and Marine Sciences, Tarbiat Modares UniversityIranian Research Institute of Plant ProtectionAbstract In Iran, native oak species are under threat from episodes of Charcoal Disease, a decline syndrome driven by abiotic stressors (e.g. drought, elevated temperature) and biotic components, Biscogniauxia mediterranea (De Not.) Kuntze and Obolarina persica (M. Mirabolfathy). The outbreak is still ongoing and the country’s largest ever recorded. Still, the factors driving its’ epidemiology in time and space are poorly known and such knowledge is urgently needed to develop strategies to counteract the adverse effects. In this study, we developed a generic framework based on experimental, machine-learning algorithms and spatial analyses for landscape-level prediction of oak charcoal disease outbreaks. Extensive field surveys were conducted during 2013–2015 in eight provinces (more than 50 unique counties) in the Zagros ecoregion. Pathogenic fungi were isolated and characterized through morphological and molecular approaches, and their pathogenicity was assessed under controlled water stress regimes in the greenhouse. Further, we evaluated a set of 29 bioclimatic, environmental, and host layers in modeling for disease incidence data using four well-known machine learning algorithms including the Generalized Linear Model, Gradient Boosting Model, Random Forest model (RF), and Multivariate Adaptive Regression Splines implemented in MaxEnt software. Model validation statistics [Area Under the Curve (AUC), True Skill Statistics (TSS)], and Kappa index were used to evaluate the accuracy of each model. Models with a TSS above 0.65 were used to prepare an ensemble model. The results showed that among the different climate variables, precipitation and temperature (Bio18, Bio7, Bio8, and bio9) in the case of O. persica and similarly, gsl (growing season length TREELIM, highlighting the warming climate and the endophytic/pathogenic nature of the fungus) and precipitation in case of B. mediterranea are the most important influencing variables in disease modeling, while near-surface wind speed (sfcwind) is the least important variant. The RF algorithm generates the most robust predictions (ROC of 0.95; TSS of 0.77 and 0.79 for MP and OP, respectively). Theoretical analysis shows that the ensemble model (ROC of 0.95 and 0.96; TSS = 0.79 and 0.81 for MP and OP, respectively), can efficiently be used in the prediction of the charcoal disease spatiotemporal distribution. The oak mortality varied ranging from 2 to 14%. Wood-boring beetles association with diseased trees was determined at 20%. Results showed that water deficiency is a crucial component of the oak decline phenomenon in Iran. The Northern Zagros forests (Ilam, Lorestan, and Kermanshah provinces) along with the southern Zagros forests (Fars and Kohgilouyeh va-Boyer Ahmad provinces) among others are the most endangered areas of potential future pandemics of charcoal disease. Our findings will significantly improve our understanding of the current situation of the disease to pave the way against pathogenic agents in Iran.https://doi.org/10.1038/s41598-024-57298-2Oak declineCharcoal diseaseZagros forestsMachine-learningSpecies distribution modelsIran
spellingShingle Meysam BakhshiGanje
Shirin Mahmoodi
Kourosh Ahmadi
Mansoureh Mirabolfathy
Potential distribution of Biscogniauxia mediterranea and Obolarina persica causal agents of oak charcoal disease in Iran’s Zagros forests
Scientific Reports
Oak decline
Charcoal disease
Zagros forests
Machine-learning
Species distribution models
Iran
title Potential distribution of Biscogniauxia mediterranea and Obolarina persica causal agents of oak charcoal disease in Iran’s Zagros forests
title_full Potential distribution of Biscogniauxia mediterranea and Obolarina persica causal agents of oak charcoal disease in Iran’s Zagros forests
title_fullStr Potential distribution of Biscogniauxia mediterranea and Obolarina persica causal agents of oak charcoal disease in Iran’s Zagros forests
title_full_unstemmed Potential distribution of Biscogniauxia mediterranea and Obolarina persica causal agents of oak charcoal disease in Iran’s Zagros forests
title_short Potential distribution of Biscogniauxia mediterranea and Obolarina persica causal agents of oak charcoal disease in Iran’s Zagros forests
title_sort potential distribution of biscogniauxia mediterranea and obolarina persica causal agents of oak charcoal disease in iran s zagros forests
topic Oak decline
Charcoal disease
Zagros forests
Machine-learning
Species distribution models
Iran
url https://doi.org/10.1038/s41598-024-57298-2
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