International Journal of Biometeorology (2022) 66:2237–2249 https://doi.org/10.1007/s00484-022-02352-9 ORIGINAL PAPER Variable climate suitability for wheat blast (Magnaporthe oryzae pathotype Triticum) in Asia: results from a continental‑scale modeling approach Carlo Montes1 · Sk. Ghulam Hussain2 · Timothy J. Krupnik2 Received: 18 January 2022 / Revised: 9 August 2022 / Accepted: 16 August 2022 / Published online: 22 August 2022 © The Author(s) 2022 Abstract Crop fungal diseases constitute a major cause of yield loss. The development of crop disease monitoring and forecasting tools is an important effort to aid farmers in adapting to climate variability and change. Recognizing weather as a main driver of fungal disease outbreaks, this work assesses the climate suitability for wheat blast (Magnaporthe oryzae pathotype Triticum, MoT) development in Asian wheat-producing countries. MoT was reported for the first time in Bangladesh in 2016 and could spread to other countries, provided that environmental conditions are suitable to spore development, distribution, and infection. With results from a generic infection model driven by air temperature and humidity, and motivated by the neces- sity to assess the potential distribution of MoT based on the response to weather drivers only, we quantify potential MoT infection events across Asia for the period 1980–2019. The results show a potential higher incidence of MoT in Bangladesh, Myanmar, and some areas of India, where the number of potential infection (NPI) events averaged up to 15 during wheat heading. Interannual trends show an increase in NPI over those three countries, which in turns show their higher interannual variability. Cold/dry conditions in countries such as Afghanistan and Pakistan appear to render them unlikely candidates for MoT establishment. The relationship between seasonal climate anomalies and NPI suggests a greater association with relative humidity than with temperature. These results could help to focus future efforts to develop management strategies where weather conditions are conducive for the establishment of MoT. Keywords Crop damage · Fungal disease · Infection model · Early warning · Climate services Introduction new diseases that have been imported (Bebber et al. 2014). This is the case of wheat blast (MoT) disease caused by The occurrence of crop diseases caused by fungal patho- the fungus Magnaporthe oryzae pathotype Triticum (MoT), gens is among the main factors affecting crop yields glob- which evolved and has been present in South America since ally (Figueroa et al. 2018). Although advances in resistant 1985 (Igarashi et al. 1986). MoT was reported for the first varieties and efficient and environmentally friendly con- time in South Asia in Bangladesh in 2016 (Malaker et al. trol options are numerous, losses associated with fungal 2016; Ceresini et al. 2018), and more recently in Southern diseases remain very important and, in some cases, dev- Africa in Zambia (Tembo et al. 2020). MoT is considered a astating (Fisher et al. 2012). The risk of crop disease out- potentially devastating fungal disease in countries where it breaks is increasing given the global trade of agricultural has been historically present, such as Brazil (Igarashi et al. commodities, which can increase the exposure of crops to 1986), Bolivia (Barea and Toledo 1996), and Argentina (Perelló et al. 2015), causing periodic and significant yield losses (Cruz et al. 2016; Duveiller et al. 2016). MoT is also * Carlo Montes an emerging threat to wheat production and food security c.montes@cgiar.org in countries where wheat is a major staple, such as in Asia 1 International Maize and Wheat Improvement Center (Islam et al. 2020a, b). (CIMMYT), Texcoco, Mexico In Bangladesh, the first MoT outbreak affected about 2 International Maize and Wheat Improvement Center 15,000 ha of wheat, with an estimated reduction of nearly (CIMMYT), Dhaka, Bangladesh 30% in production in 2016 (Islam et al. 2020a, b; Yesmin Vol.:(012 3456789) 2238 International Journal of Biometeorology (2022) 66:2237–2249 et al. 2020). Although subsequent outbreaks have not been climate variables (e.g., atmospheric humidity and tempera- recorded, the disease remains present in Bangladesh with ture), provided that parameters are adequately set for a spe- low to moderate severity when detected (Singh et al. 2021). cific disease (Bregaglio et al. 2012; Bregaglio and Donatelli The impacts of MoT on wheat yields and grain quality can 2015). In the case of MoT, Fernandes et al. (2017) devel- be devastating for susceptible cultivars, but they can vary oped a wheat blast–specific model aiming at implementing greatly in response to other factors such as weather con- an early warning system for Brazil, which was applied and ditions, growth stage, or planting date (Cruz and Valent evaluated at the local level using a single-location approach 2017). In this way, when weather conditions are suitable and then extended to Bangladesh (Fernandes et al. 2021). for MoT infection, grain yield losses can range from slight The need for decision-making tools for farmers from other to total (Duveiller et al. 2011; Singh et al. 2021), as it has wheat-growing regions in Asia has been emphasized later been reported in South American countries such as Brazil or (Singh et al. 2020), given the potential risk for the range of Bolivia, where yield losses have reached up to 100% (Gou- disease expansion (Islam et al. 2020a, b). In this context, the lart and Paiva 1992; Barea and Toledo 1996). aim of this work is to provide a large-scale and long-term Although there are still no official reports of the presence assessment of the climate suitability for MoT development of MoT in others countries than Bangladesh in Asia, studies over wheat-growing areas of Asia in terms of mean histori- of climate suitability for MoT have suggested that it may cal (1980–2019) weather conditions and interannual vari- spread to areas with humid and warm climates in neigh- ability, based on the analysis of the results obtained from boring countries such as India or Pakistan (Motaleb et al. high-resolution meteorological data and a generic infection 2018a). Research has also suggested that Ethiopia (Duveiller model. The results from this work, which represent an esti- et al. 2011) and the USA (Cruz et al. 2016) may be risk- mate of the potential pressure that can be exerted by MoT prone. In these regions, both seed-born and air-born spore driven by background meteorological conditions, can con- propagation, suitable weather conditions, and disease sus- tribute to the understanding of the spatial patterns in suitable ceptible cultivars can act synergistically to increase the risk weather conditions for MoT and their main large-scale driv- of disease outbreak, potentially threatening food security ers, and can potentially provide guidance for future efforts (Ceresini et al. 2018). These risks have motivated a number and regional prioritization in the development of early warn- of efforts to monitor pathogen presence (Fernandes et al. ing systems based on weather monitoring and forecasting. 2021; Islam et al. 2016; Yesmin et al. 2020), and to develop management strategies including resistant varieties (Hos- sain et al. 2019), chemical and nonchemical control methods Data and methods (Singh et al. 2021), and early warning systems (Fernandes et al. 2021; Kim and Choi 2020). Study area Multiple tools have been developed for the monitoring and forecasting of fungal disease outbreaks based on field Eight Asian countries were identified based on the extent of observations or empirical and deterministic models com- wheat cultivation and consumption and the recent emergence bining weather variables to generate early warnings of the of wheat blast disease in 2016 in Bangladesh, which are sum- potential risk of disease outbreaks (Launay et al. 2014). Con- marized in Table 1 for 2019. In alphabetic order, these include sidering MoT in Asia, studies of its potential spread have Afghanistan, Bangladesh, Bhutan, China, India, Myanmar, been carried out using monthly climate statistics (e.g., Mot- Nepal, and Pakistan. In these countries, winter wheat is planted aleb et al. 2018a) or limited temporal and spatial domains in the autumn, with a long vegetative stage during the dry sea- (e.g., Kim and Choi 2020). No large-scale, continental, and son in winter, and the reproductive stage generally occurring high-resolution assessments have conversely been carried with the onset of the spring. In addition, spring wheat is culti- out in Asia. However, given increasing availability of envi- vated in areas with mild winters such as in India, and at eleva- ronmental data and computing capacities, the use of simula- tion in the Himalayas, where wheat is sown in autumn and har- tion models to diagnose and forecast favorable conditions for vested after the winter without vernalization, though land area the development of crop diseases has grown in importance devoted to spring wheat is limited in South Asia (Curtis 2002; (Donatelli et al. 2017). Krupnik et al. 2021). For this reason, this study focuses on Diagnosis and applications vary from regional assess- winter wheat as the predominant crop. Wheat is a major staple ments of climate suitability (Bebber et al. 2017), sensitiv- food in Afghanistan and Pakistan, with a total production of ity analysis to environmental drivers and parameterizations 4.9 and 24.3 Mt (million tonnes) over 2.3 and 8.7 Mha (million (Bregaglio et al. 2012), and future projections in risks asso- ha) in 2019, respectively (Fig. S1; FAOSTAT 2021). Wheat ciated with climate change (Bregaglio et al. 2013). The latter consumption has been increasing progressively in India, Bhu- suggested that the suitable conditions for the establishment tan, Myanmar, and Bangladesh, becoming the second most of fungal diseases can be well captured by models forced by important staple food after rice (Motaleb et al. 2018b). China 1 3 International Journal of Biometeorology (2022) 66:2237–2249 2239 Table 1 Main wheat production Country Production (tonnes) Area harvested (ha) Aver- statistics for the eight Asian age yield countries considered in this (tonnes/ha) study for the year 2019. Values in brackets correspond to the Afghanistan 4,890,000 (39,767) 2,334,000 (− 372) 2.095 (0.02) slope of the linear fit of the corresponding statistics for the Bangladesh 1,016,811 (24,511) 330,348 (8360) 3.078 (0.04) period 1961 through 2019. Data Bhutan 1319 (− 18) 1004 (− 68) 1.314 (0.02) from FAOSTAT 2021 China 133,596,300 (2,079,597) 23,730,000 (− 37,782) 5.630 (0.09) India 103,596,230 (1,612,311) 29,318,790 (297,338) 3.533 (0.05) Myanmar 110,663 (2125) 58,866 (289) 1.880 (0.02) Nepal 2,005,665 (34,027) 703,992 (12,368) 2.849 (0.03) Pakistan 24,348,983 (412,302) 8,677,730 (73,567) 2.806 (0.04) is the world’s largest wheat producer, with 133.5 Mt grown Tmin, Tmax, and Topt are the minimum, maximum, and opti- on 23.7 Mha in 2019; India is the second largest producer, mum temperatures for infection, respectively. These cardi- growing 103.6 Mt in 2019 on 29.3 Mha (FAOSTAT 2021). nal temperatures were taken from Cruz et al. (2016), who Bangladesh conversely is a net importer of wheat, producing suggested the following values for MoT: Tmin = 10  °C, 1 Mt over 0.33 Mha in 2019, cultivated exclusively during Tmax = 32 °C, and Topt = 27.5 °C. As an example, Fig. S2 the winter after monsoon season rice fields are drained. In shows the resulting shape of f(T), where, following a slow Nepal, wheat is grown in the low-lying Terai (up to 500 m response, exponential increasing response to temperature is above sea level) and in the Himalayan mid-hills (Morris et al. observed between Tmin and around 20 °C, which turns from 1994; Krupnik et al. 2021), with a total of 2 Mt produced from almost linear to a decreasing-rate increment until Topt, to 0.7 Mha in 2019. In Myanmar, more than 90% of the wheat then drops rapidly until f(T) = 0 at Tmax. The air temperature is found in the hilly Sagaing and Shan states (USDA, 2019), response f(T) is subsequently scaled to the wetness dura- with a production of 110,000 tonnes from 59,000 ha in 2019. tion requirement for infection according to the following In Bhutan, wheat is also produced at elevation, reaching 1319 relationship: tonnes from 1004 ha in 2019 (Tshewang et al. 2017). { WDmin WD , if min < WD W(T) = f (T) f (T) max , Modeling potential wheat blast infections (2) 0, elsewhere Model description where W(t) (dimensionless, values from 0 to 1) corresponds to the wetness response function, and WDmin and WDmax The generic infection model developed by Magarey et al. (hours), taken as 12 and 24, respectively (Cruz et al. 2016), (2005) was used to assess the climate suitability of MoT infec- are the minimum and maximum leaf wetness duration tions. This model has been previously applied for large-scale requirement for infection, respectively. Therefore, when the studies of fungal disease infections given the biological sig- infection models use hourly forcing data, it is necessary to nificance of its parameterizations and simple implementation account for the number of hours that may interrupt a wet (Bregaglio et al. 2012, 2013). The model considers both the period without terminating the infection process, as Magarey effect of hourly air temperature and plant surface wetness (or et al. (2005) explained. For this, the model considers the relative humidity) duration on the development response of a impact of critical dry periods through the parameter D50 generic fungal pathogen by using two functions describing its that is calculated as: sensitivity to air temperature and humidity. The model uses the { air temperature response function proposed by Yan and Hunt W W 1 +W2, ifD ≤ D50 sum = , (3) (1999), which combines a set of pathogen’s cardinal tempera- W1,W2, elsewhere tures to estimate the shape of the response as: where Wsum is the sum of the surface wetting periods and W1 ( )( ) and W2 indicate two wet periods separated by a dry period T (Topt−Tmin)∕(Tmax−Topt ) max − T T − Tmin f (T) = , (D, in hours). As in Magarey et al. (2005), D50 is defined as Tmax − Topt Topt − Tmin the duration of a dry period at relative humidity < 95% that (1) will result in a 50% reduction in disease compared with a where f(T) (dimensionless, values from 0 to 1) is the temper- continuous wetness period. Therefore, if D > D50, the model ature response function; T (°C) is the hourly air temperature; considers the two wet periods as separate wetting events. 1 3 2240 International Journal of Biometeorology (2022) 66:2237–2249 When the plant surfaces are wet and f(T) > 0, the model are obtained from dewpoint (Td) temperature and actual air assumes that inoculant is present in the environment and temperature (T), respectively (Allen et al. 1998): adds a cohort of spores. Infection events are triggered when ( ) 17.27×Td the value of Wsum ranges between WDmin and WDmax (Brega- e = 0.611 × exp 237.3+Td (4) a glio et al. 2012). Although the values of the D50 parameter were gathered by Magarey et al. (2005) for a number of ( ) 17.27×T species of fungal diseases, D50 has not yet been calibrated e = 0.611 × exp 237.3+T (5) s for MoT. We however included a value of D50 of 4, which was used by Bregaglio et al. (2013) for the assessment of ea potential infections of Pyricularia oryzae, a MoT anamorph, RH = 100 × e (6) s in Europe (Martínez et al. 2019). The above set of equations were solved for the wheat heading period, which was esti- with ea and es are expressed in kPa, and temperatures in mated using a phenological model based on thermal time °C. Maps of the seasonal climatology of these variables are accumulation, as presented below. provided in Fig. S3. Representing wheat distribution and phenology Infection model forcing The spatial distribution of wheat area was represented using Multiple global gridded climate products are currently avail- the Spatial Production Allocation Model SPAM 2010 v1.0 able, which can be potentially used to model and diagnose global crop production data product developed by the Inter- crop diseases. However, meteorological information must be national Food Policy Research Institute (IFPRI) (Wood- provided at appropriate temporal and spatial scales, given Sichra et  al. 2016; International Food Policy Research the behavior of crop pathogens. Among the meteorological Institute (IFPRI) 2019). This product provides statistics on variables most used for crop disease modeling are air tem- crop production by merging sub-national statistics, satellite- perature, precipitation, relative humidity, and leaf wetness derived land cover, environmental crop suitability, popula- (Donatelli et al. 2017). More complex and highly demanding tion, cropping systems, and markets, among other variables. in computer resources, transport-based Lagrangian models The operational product is generated after the crop produc- require wind speed and direction to calculate fungal spores’ tion data derived from the above-mentioned information trajectories and deposition (Meyer et al. 2017). is aggregated into a regular grid of spatial resolution of Most global gridded climate products are provided at around 10 km × 10 km using a cross-entropy method (You daily time-steps as the higher temporal resolution, which and Wood, 2006). In this work, the original data grid was may be limiting for the simulation of crop diseases. bilinearly interpolated to the 0.25° × 0.25° climate forcing Although there are methods to statistically disaggregate resolution and then converted into a binary mask (Fig. S4). daily time series to hourly values via empirical models or MoT infections were estimated for the phenological weather generators (Bregaglio et al. 2010), their accuracy period from heading to the end of the reproductive phase can be limited by the available historical data and their (maturity). The starting and ending dates of this suscepti- implementation can be difficult when it comes to large ble period were calculated using crop growth modeling and datasets. This study used hourly data from the last genera- global climate products. Thus, the spatially explicit critical tion European Centre for Medium-Range Weather Forecasts dates necessary for bounding the modeling time window are (ECMWF) ERA5 global atmospheric reanalysis as mete- sowing date, emergence, beginning of the heading stage, orological observations to force the infection model. This and beginning of physiological maturity. After represent- product is provided at an hourly time scale with a horizontal ing the spatial distribution of wheat, the key phenological resolution of 0.25° × 0.25° (~ 31 km), covering the period dates were stated. First, winter wheat sowing dates were 1979 to present for single (surface) and multiple vertical obtained from the interpolated Crop Calendar Dataset of levels (Hersbach et al. 2020). ERA5 is generated using a Sacks et al.’s (2010) product, which provides 5′ × 5′ spatial 4D-Var data assimilation scheme to optimally combine out- resolution global dates of crop sowing and harvest dates rep- puts from the ECMWF Integrated Forecasting System with resentative of the year 2000. Here, the original resolution satellite and ground observations. We utilized the hourly dataset was bilinearly aggregated to match the 0.25° × 0.25° ERA5 air and dewpoint temperature at surface level (2 m ERA5 resolution (Fig. S4). height), and rainfall data for the period from January 1980 The wheat heading period was estimated using point- through December 2019. Relative humidity (RH) for the based simulations with the CSM-CROPSIM-CERES-wheat infection model was calculated using the widely used equa- model, embedded in the Decision Support System for Agro- tion involving actual and saturated vapor pressure, which technology Transfer (DSSAT) v.4.6 (Jones et al. 2003). 1 3 International Journal of Biometeorology (2022) 66:2237–2249 2241 CROPSIM-CERES simulates wheat phenology according to the Zadoks stages (Zadoks et al. 1974) as a function of growing degree day accumulation and accounting for envi- ronmental stresses, vernalization, and photoperiod effects. Simulations were performed over a set of 163 wheat-grow- ing locations belonging to the International Wheat Improve- ment Network (IWIN; Reynolds et al. 2017) for the period 1979 through 2019 (Fig. S5). The meteorological forcing (air temperature, solar radiation, rainfall, relative humidity, wind speed) was performed using ECMWF’s AgERA5 prod- uct (Copernicus Climate Change Service (C3S), 2019), a statistically downscaled (0.1° × 0.1°) daily version of ERA5. Global soil profiles from the HC27 product (Koo and Dimes 2010) were used to provide soil physical and chemical prop- erties to CROPSIM-CERES. Genetic coefficients necessary for wheat simulations were set based on the cultivar distribu- tion over the International Maize and Wheat Improvement Center’s (CIMMYT’s) wheat mega-environments, which correspond to homogeneous agroecological zones for wheat cultivation (Pequeno et al. 2021). A comparison between Fig. 1 Flow diagram of the modeling approach for number of poten- CROPSIM-CERES simulated number of days from sow- tial infections (NPI) of MoT. See text for acronyms and product ing to anthesis and IWIN observations showed a normalized names root mean square error of 7.6% (data not shown). Finally, using sowing dates from Sacks et al. (2010), simulated dates series. Anomalies were obtained by removing the corre- of anthesis and maturity were obtained for every location, sponding long-term average. and the heading date was assumed to occur 10 days before anthesis. Both heading and maturity dates were bilinearly interpolated to 0.25° × 0.25° working spatial resolution of Results the SPAM product (Fig. S5). A flow diagram schematically describing the main steps of the modeling approach is shown Mean patterns and interannual variability in Fig. 1. of number of potential MoT infections Figure 2a shows the map of interannual mean total seasonal Analysis NPI in Asia. The mean seasonal NPI is 7.5 (median of 6) and interquartile range from 4 to 9 (Fig. 3a). In Fig. 2a, while Data analysis involved three analytical steps. The first step 57.6% of SPAM wheat grid cells present suitable conditions focused on the quantification of the average and interan- for MoT, 6.7% of them present favorable conditions during nual variability (1980–2019) in the weather-driven number all 39 years studied. The map shows a spatial distribution of of potential infections (NPI) of MoT summarized for all NPI indicating higher climate suitability for MoT develop- selected countries, except for Bhutan, where model results ment over areas near the ocean over the southern fraction of showed non-suitable climate conditions for wheat blast the domain, such as in Bangladesh, some areas of West Ben- development. The interannual trends (slope of the linear fit) gal and Bihar India, and in Myanmar. The model suggests in NPI were also evaluated, and their statistical significance that MoT can also establish over large areas of central India, was assessed using the non-parametrical Mann–Kendall test Myanmar, and China, though at lower NPI levels. Con- (Kendall, 1955) at a confidence level of 0.05. In the second versely, other wheat-producing regions have air temperature step, the covariability between NPI and climate variables and humidity ranges that would not represent favorable con- was assessed. This was performed by computing the Pear- ditions for MoT outbreaks, including most areas in Afghani- son correlation coefficient between pairs of detrended time stan, Pakistan, and central China. Figure 2b shows the inter- series of NPI and air temperature, relative humidity, and annual variability (standard deviation) of potential infections rainfall anomalies. Lastly, a composite analysis of anomalies in Asia, where a strong interannual variability is observed in of the above-presented climate variables was performed for areas of higher incidence (Bangladesh, Myanmar), but also the years of highest MoT incidence predicted by the model, a southward increase in potential infection risks in India. taking the upper quartile (75th percentile) of the NPI time Similarly, interannual variability of NPI shows a wider 1 3 2242 International Journal of Biometeorology (2022) 66:2237–2249 Fig. 2 Maps of a mean and b interannual variability repre- sented by the standard deviation (1980–2019) of the number of Magnaporthe oryzae patho- type Triticum (MoT) potential infections (NPI) in Asia. Black dots represent grid cells with presence of wheat but where the climate appears to not be suit- able for MoT outbreaks. P99th is the 99% percentile range over the areas of higher MoT potential incidence (e.g., shown in Fig. 2a, although only a small fraction is statisti- Bangladesh). The southward increasing pattern in India and cally significant according to the Mann–Kendall test. Posi- Myanmar suggests that the pressure of the disease could tive trends are dominant in Bangladesh, central Myanmar, be much higher than the average conditions during more and over portions of the Indo-Gangetic Plains (IGP) of India. favorable years for its development, so long as sufficiently Decreasing trends are observed further south over warmer susceptible wheat cultivars are grown and alternative hosts areas of India and in Myanmar’s delta, where recent tem- maintain inoculum outside the wheat-growing season. The perature trends may be above the maximum MoT develop- distributions of total multi-year NPI cases and NPI normal- ment temperature in the model (IPCC 2021). ized by the corresponding infected area and aggregated by country are presented in Fig. 3a and b, respectively. There is Seasonal climate anomalies and number a considerable variation in the mean and spread of the dis- of potential MoT infections tribution of normalized NPI across countries. However, it is clear that Bangladesh is the country with the highest relative The relationship between NPI and seasonal anomalies potential MoT pressure associated with climate, followed by (from wheat heading to maturity) of air temperature (T), India and Myanmar, which present similar disease risk sce- relative humidity (RH), and total rainfall (R) is described in narios, and then in Nepal, China, Pakistan, and Afghanistan. Fig. 5a–c, which show the correlation coefficient calculated The long-term interannual trends in seasonal total NPI are between NPI and these variables. The correlation map of displayed in Fig. 4, including their statistical significance. NPI and T shows that most of the grid points with suitable Our model outputs suggest generally increasing trends in climate conditions for MoT described in Fig. 2 do not present NPI that concentrate over areas of higher MoT pressure statistically significant correlations. This is likely due to the 1 3 International Journal of Biometeorology (2022) 66:2237–2249 2243 suitability considered in the model, indicative of reduced infection risk potential. On the other hand, the correlation between NPI and RH (Fig. 5b) is much more apparent than with temperature; this is indicative of the importance of RH conditions for the potential development of the disease. In this case, strong positive correlations are observed over Bangladesh, Myanmar, and some areas of India, which cor- respond to those of higher MoT pressure (Figs. 2 and 3). A very weak correlation between NPI and total rainfall is observed in Fig. 5c for the whole geographical domain. Since the calculation period falls in general within the dry season (Fig. S6), our models suggest that precipitation may not be a significant determining factor of the incidence of MoT at the scales of the present work, as other factors asso- ciated with atmospheric water vapor transport might be more relevant (Ahmed et al. 2020). However, the 2016 outbreak of MoT in Bangladesh has been associated with strong storm events during the dry season (Singh et al. 2021), which is not captured by a correlation-based analysis. The maps of mean composite anomalies of T, RH, and R calculated for the years of the highest infection events, repre- sented by the upper quartile of NPI, are displayed in Fig. 5d–f. Figure 5d shows an area of negative temperature anomalies in northern Bangladesh that was already observed with high interannual correlations in Fig. 5a. In general, both India and Myanmar present a pattern of anomalies that are not very clear, although they in general follow what is observed in terms of correlations (Fig. 5a). Conversely, RH shows a spa- tial distribution (Fig. 5e) that appears to be consistent with the interannual correlations (Fig. 5b), where anomalously high seasonal NPI is associated with positive anomalies in RH, appearing again as a variable with high discriminatory power for modeled NPI. Figure 5f shows that high incidence of MoT is likely to be associated with negative precipitation anomalies. The latter suggests that, despite the null correlation between both variables, drier-than-normal winters may tend to be more favorable for MoT outbreaks. Fig. 3 a Histogram of multi-year number of potential MoT infections Discussion (NPI) in Asia; P25% and P75% are the corresponding percentiles. b Boxplots of interannual distribution of NPI. In b, the red central mark Climate suitability for MoT in Asia shows the median and the box edges are the 25th and 75th percen- tiles; dashed lines extend to the most extreme values not considered outliers, and outliers are plotted individually (× signs) Assuming the presence of inoculum and susceptible culti- vars, the primary goal of this study was to provide a general and objective overview of the background climate conditions scaling used in the temperature response function (Eq. 1), for the development of MoT over a region where wheat cul- which implies a non-linear relationship between temperature tivation is important for food security (Yonar et al. 2021), and NPI. However, a small area in northern Bangladesh with and whose agricultural landscape is described as being relatively high MoT pressure (Fig. 2) has significant negative highly exposed to the shocks associated with weather and correlations. This area exhibits high temperatures during the climate variability (Amarnath et al. 2017). At the time of wheat heading period (Fig. S6), which may imply a higher writing, MoT has only been officially reported in Bangladesh frequency of hours with the temperature above the range of (Malaker et al. 2016), though unofficial reports of the disease 1 3 2244 International Journal of Biometeorology (2022) 66:2237–2249 Fig. 4 Map of interannual trends (1980–2019) in NPI over Asia. Black dots represent areas where linear trends are statisti- cally significant (α = 0.05) according to the Mann–Kendall test have also been published in the popular media in eastern On the other hand, we also observed increasing NPI risks in India, prompting the temporary banning of wheat cultivation northwestern India. This result could potentially be associ- in some areas (cf. Islam et al. 2020a, b); our modeling efforts ated with irrigation, which is intensively applied to wheat also suggest high disease pressure risks, though not always on over 80% of the land area devoted to rice–wheat rotations with significant and positive interannual trends, potentially in northwestern India (Hussain et al. 2003; Jain et al. 2017; backing the consistent but spatially variable incidence and Ram et al. 2013;), which could contribute to land surface severity of MoT observed in this country between 2017 and cooling during the pre- and post-monsoon period (Mishra present (CSISA 2021). The reasons for the variable nature et al. 2020). Intensified use of irrigation on the other hand of infections observed in Bangladesh and South Asia remain has also increased evaporation, increasing actual water vapor unclear; though recognizing weather conditions as a major pressure (Tuinenburg et al. 2014), which can determine an driver of fungal disease outbreaks (Bregaglio et al. 2012; increase in relative humidity creating conditions that are Juroszek et al. 2019), improved knowledge regarding the more suitable for MoT development (Bregaglio et al. 2012). environmental suitability for the establishment of MoT can Additionally, our scenarios suggest that high incidence of aid in anticipating the development of disease management MoT is likely to be associated with negative precipitation strategies. These include but are not limited to the deploy- anomalies. The latter could be associated with the regulatory ment of new resistant varieties, cultural control methods, and effect of rainfall on air temperature, which affects relative the use of early warning systems in wheat regions where the humidity during a period of the year where precipitation disease is a potential threat for food security. events are sporadic. However, further analysis is necessary The results highlight the importance of spatial variabil- to validate this hypothesis. ity in the climate suitability for the establishment of MoT On the other hand, results suggest that wheat-producing in Asia, with a higher potential observed in Bangladesh, regions with low temperature and humidity in Afghani- Myanmar, and some areas of India, where low elevation, sea stan, Pakistan, or some areas of India are unlikely to be proximity, or regional low-level circulation can favor factors at significant risk for MoT outbreaks, as climatic regime such as atmospheric water transport (Ahmed et al. 2020). appears to be out of the range for the disease development Using a methodologically similar approach, a similar spa- (Magarey et al. 2005; Cruz et al. 2016). According to the tial pattern in the suitability of rice leaf blast (Magnaporthe observed relationship between interannual variability in oryzae pathotype Oryzae) driven by summer weather over NPI and the selected climate variables, a clear association North India was described by Viswanath et al. (2017) for between anomalies of RH and NPI was observed, which India. At the same time, regions that appear to have higher is explained by the structure of the infection model. This potential risks for infection in our model are also associated observation confirms those of Kim and Choi (2020) and with higher interannual variability. This appears to reflect Fernandes et al. 2017) that suggested that this variable in literature on MoT from South America (Fernandes et al. could be potentially used for the development of seasonal 2017) and observations in Bangladesh (CSISA 2021) that the early warning systems. Indeed, recent efforts to develop disease is irregularly periodic, increasing in incidence and weather-based early warning systems in Bangladesh and severity only during years of higher favorable conditions. Brazil (e.g., Fernandes et al. 2021; http://b eatth eblas tews. 1 3 International Journal of Biometeorology (2022) 66:2237–2249 2245 Fig. 5 a–c Maps of local Pearson correlation coefficient between a mean air temperature, b relative humidity, and c total rainfall asso- number of potential infections (NPI) and a mean temperature (T), b ciated with the upper quartile of NPI. Only grid cells exceeding the relative humidity (RH), and c total rainfall (R). Only significant cor- 95% confidence interval are displayed in d–f relations at the 10% level are displayed. d–f Composites of seasonal net/) rely largely on humidity and temperature as driv- Limitations and uncertainties ing variables. Nevertheless, the association between NPI and climate anomalies seems to be clearer when using The approach used in this study considers the combination a composite approach, which could open the possibility of multiple sources of secondary information and modeling of generating probabilistic seasonal forecasts of favorable (cropping calendars, phenology, potential infections, etc.). conditions for MoT outbreaks. The latter could be further This in turn implies multiple sources of uncertainty and explored using indices from large-scale drivers (El Niño/ limitations that should be considered in order to improve La Niña) and suitable lead times. In addition, although the understanding of the conditions conducive to the devel- most of the area of the geographical domain studied did opment of crop diseases, including future projections in cli- not exhibit statistically significant trends, areas that exhibit mate. For instance, the generic infection model considers the show positive trends in NPI that could increase in response moment when favorable weather conditions for the devel- to projected climate change scenarios, which should be opment of MoT are fulfilled to declare an outbreak. How- addressed in future studies. ever, other complex disease-host interaction processes could 1 3 2246 International Journal of Biometeorology (2022) 66:2237–2249 determine the successful establishment of the disease, which products of key phenological stages. Similarly, although are not considered in the model, which also assumes that the SPAM dataset (Wood-Sichra et al. 2016; International inoculant is present in the environments being studied (e.g., Food Policy Research Institute (IFPRI) 2019) is widely Bregaglio et al. 2012, 2021). Additionally, other relevant used (e.g., Joglekar et al. 2019; Yu et al. 2020), it is par- variables that have been considered in other similar works tially based on administrative report data for 2005 and has could be included. For instance, the “wash-off” effect of not been thoroughly ground-truthed and as such there may spores from spikes by rainfall above a specific intensity has be spatial over- and under-estimation of wheat cultivation been considered by Fernandes et al. (2017), which can be area. For example, Myanmar has a declining trend and less relevant over more where significant rains occur during the than 100,000 ha of wheat (FAOSTAT 2021; USDA PS&D heading wheat period. Another source of uncertainty are the 2022), while the SPAM product suggests a cultivation area model parameters, and specifically the D50 parameter used of around 85,500 ha, and a more southern distribution in Eq. 3, which was extracted from similar fungal species of cultivation than other sources suggest (USDA PS&D (Puccinia sp. and Bipolaris sp.) in rice and wheat. Although 2022). Future researchers may therefore consider making this can lead to errors, Bregaglio et al. (2012) found that use of satellite-derived estimates for wheat phenology to results are not very sensitive to the values of D50 for other complement this data source, for example, using methods fungal diseases. We however conducted a simple sensitiv- described by Jain et al. (2017). Yet despite these potential ity analysis, S7, that was performed using a set of values of inconsistencies, our model outputs still provide a useful D50, from “sensitive” to “insensitive” to dry interruptions indication of the potential for MoT infection risks, and can according to Magarey et al. (2005), presented in Fig. S7, therefore be used to help in crop planning and zoning, in which suggests that the calculated NPI are not very sensitive addition to integrated pest management efforts, although to variations in D50 values. In any case, a global sensitiv- care should be exercised when interpreting our results. ity and uncertainty quantification analysis would provide a better understanding of the model structure and sensitivity to parameters and threshold values (Bregaglio et al. 2012), which is, however, out of the scope of this work. Conclusions In addition, and in spite of using phenology dates that are comparable to other works (e.g., Liu et al. 2020), the The sudden, unexpected arrival of wheat blast disease in use of fixed planting and heading/maturity dates may rep- Bangladesh in 2016 underscores the risk associated with resent a source of error during, for instance, anomalously this disease. Although formally reported in Bangladesh at warm/cold years, in which the phenological stages can the time of writing, there is a lack of clarity on the potential be accelerated/delayed. The latter may represent a limi- distribution of the MoT species and its effect on wheat cul- tation when developing early warning systems based on tivation throughout the Asian continent. Our results suggest seasonal climatic forecasts, which currently provide infor- a differential suitability for the development of MoT—and mation on a monthly or longer scale. Moreover, we relied a large interannual variation in some key wheat-producing on a single, though comprehensive data source for plant- areas—across Asia. The contrasting potential risk of MoT ing dates from the interpolated Crop Calendar Dataset of between Bangladesh, Myanmar, and some states within Sacks et al. (2010). Although widely used, this dataset India, with infection events averaging up to 15 during the may have inaccuracies with observed planting dates, which wheat spike, and limited risks in Afghanistan and Pakistan, can in turn affect phenological development. For exam- and in central China, could allow focusing efforts to increase ple, this dataset shows quite late wheat sowing dates into the resilience and preparation of farmers for potential December in the north western IGP, and specifically in future biotic shocks. Importantly, our results also highlight the Indian states of Haryana and Punjab (Fig. S4). These a stronger association between relative humidity and MoT locations however tend to be associated with earlier plant- infection than with temperature regime. Accordingly, future ing than in the eastern IGP (Lobell et al. 2013; Jain et al. improvements should further investigate if and how rela- 2017). The reasons for the lack of congruence between tive humidity can be used to simplify data requirements and the Sacks et al. (2010) dataset and observations are not modeling efforts. New research should also focus on includ- clear, although future studies should query the relationship ing more complex pathogen-plant interaction processes, between crop establishment dates and disease incidence, dynamic wheat phenology, source-sink relationships, and in an effort to identify if and how MoT risks could be wind dispersal patterns, higher resolution climate forcing for mitigated through manipulation of sowing dates. Remote historical and future assessments. Although still preliminary sensing–based regional sowing date estimations based in nature, our results nonetheless may aid in the develop- on the seasonality of satellite time series such TIMESAT ment or refinement of early warning systems and agricultural (Jönsson and Eklundh, 2004) could help to generate global climate services associated with MoT and similar diseases. 1 3 International Journal of Biometeorology (2022) 66:2237–2249 2247 Supplementary Information The online version contains supplemen- Bregaglio S, Donatelli M, Confalonieri R, Orlandini S (2010) An inte- tary material available at https://d oi.o rg/1 0.1 007/s 00484-0 22-0 2352-9. grated evaluation of thirteen modelling solutions for the genera- tion of hourly values of air relative humidity. Theor Appl Climatol Acknowledgements The authors gratefully acknowledge the ECMWF 102:329–438 for providing the ERA5 data. CM acknowledges Ernesto Girón for Bregaglio S, Cappelli G, Donatelli M (2012) Evaluating the suitability his support on CROPSIM-CERES simulations. The valuable com- of a generic fungal infection model for pest risk assessment stud- ments and suggestions from two anonymous reviewers are deeply ies. Ecol Model 247:58–63 acknowledged. Bregaglio S, Donatelli M, Confalonieri R (2013) Fungal infections of rice, wheat, and grape in Europe in 2030–2050. Agron Sustain Dev 33:767–776 Funding Funding for this research was supplied by USAID and the Bill and Melinda Gates Foundation (BMGF) through the Cereal Systems Bregaglio S, Donatelli M (2015) A set of software components for Initiative for South Asia (CSISA), and the Climate Services for Resil- the simulation of plant airborne diseases. Environ Modell Soft ient Development (CSRD) in South Asia project, supported by USAID. 72:426–444 Additional support was provided by the CGIAR Research Program on Bregaglio S, Willocquet L, Kersebaum KC, Ferrise R, Stella T, Ferreira Climate Change, Agriculture and Food Security (CCAFS; https://c cafs. TB, Pavan W, Asseng S, Savary S (2021) Comparing process- cgiar. org), by the CGIAR Regional Integrated Initiative Transforming based wheat growth models in their simulation of yield losses Agrifood Systems in South Asia, or TAFSSA (https:// www. cgiar. org/ caused by plant diseases. Field Crop Res 265:108108 initia tive/2 0-t ransf ormin g-a grifo od-s ystem s-i n-s outh-a sia-t afssa/), and Ceresini PC, Castroagudín VL, Rodrigues FA, Rios JA, Eduardo by the CGIAR Foresight and Metrics to Accelerate Inclusive and Sus- Aucique-Pérez C, Moreira SI, Alves E, Croll D, Nunes Macie JL tainable Agrifood System Transformation initiative (https://w ww.c giar. (2018) Wheat blast: past, present, and future. Annu Rev Phyto- org/ initi ative/ 24- fores ight- and- metri cs- to- accel erate- inclu sive- and- pathol 56(427):456 sustai nable-a grifo od-s ystem-t ransf ormat ion/). The contents expressed Copernicus Climate Change Service (C3S) (2019) Data Stream 2: herein are those of the author(s) and do not necessarily reflect the AgERA5 historic and near real time forcing data. Product User views of USAID, BMGF, CGIAR, or the US government, and shall not Guide and Specification. Copernicus Climate Change Service Cli- be used for advertising or product endorsement purposes. mate Data Store (CDS). Online: http://d atast ore.c opern icus-c lima te.e u/d ocume nts/s is-g lobal-a gricu lture/C 3S422 Lot1.W EnR.D S2_ Produ ctUse rGuid eSpec ifica tion_ v2.2. pdf. Accessed 10 Jan 2022 Open Access This article is licensed under a Creative Commons Attri- Cruz CD, Magarey RD, Christie DN, Fowler GA, Fernandes JM, bution 4.0 International License, which permits use, sharing, adapta- Bockus WW, Valent V, Stack J (2016) Climate suitability for tion, distribution and reproduction in any medium or format, as long Magnaporthe oryzae Triticum pathotype in the United States. as you give appropriate credit to the original author(s) and the source, Plant Dis 100:1979–1987 provide a link to the Creative Commons licence, and indicate if changes Cruz CD, Valent B (2017) Wheat blast disease: danger on the move. were made. 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