A Standard Area Diagram Set for Assessing Dragon Fruit (Hylocerus Spp.) Stem Canker Severity Caused by Neoscytalidium Dimidiatum

doi:10.21203/rs.3.rs-3750801/v1

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A Standard Area Diagram Set for Assessing Dragon Fruit (Hylocerus Spp.) Stem Canker Severity Caused by Neoscytalidium Dimidiatum

https://doi.org/10.21203/rs.3.rs-3750801/v1

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Dragon fruit canker (DFC) disease caused by the fungus Neoscytalidium dimidiatum poses a significant threat to yield and fruit quality in cultivating dragon fruit (Hylocerus spp.). Accurate assessment of canker severity is crucial for determining the effectiveness of the management strategies for controlling this disease. We developed a standard area diagram set (SADs) consisting of nine levels of disease severity (0.3 to 60%) and subsequently validated based on the patterns and distribution of the symptoms. For the validation, eighteen raters with no prior experience in disease assessment were recruited to estimate the severity of canker symptoms on 50 stems/cladodes of dragon fruit before and after the use of SADs. Both accuracy and precision were improved when they used the SADs. Statistical parameters for the 18 raters were as follows: bias coefficient factor (C_b) without SADs = 0.791, with SADs = 0.982; correlation coefficient (r) without SADs = 0.884, with SADs = 0.918; Lin's concordance correlation coefficient (ρc) without SADs = 0.702, with SADs = 0.902. Estimates were also more reliable by using the SADs: inter-rater coefficient of determination (R²) without SADs = 0.749, with SADs = 0.810. The newly developed SADs provide a practical, standardized tool for assessing dragon fruit canker severity, aiding researchers and growers in more accurate disease monitoring, yield loss estimation, intervention planning, and control measure evaluation.

pitahaya

dragon fruit canker

diagrammatic scale

phytopathometry

disease assessment

Dragon fruit, also known as ‘pitaya’ or ‘pitahaya’, is a minor tropical fruit crop that has become an economically important crop on a global scale due to its health benefits, profitability potential, minimal maintenance requirements, adaptability to diverse climates, and strong market demand (Hossain et al., 2021; Merten, 2003; Nangare et al., 2020; Wakchaure et al., 2021). Over the past decade, many countries, including Vietnam, China, Thailand, Malaysia, Indonesia, Israel, Ecuador, Colombia, Nicaragua, Brazil, and the United States, have expanded dragon fruit cultivation in response to increasing global demand for fresh and processed dragon fruits (Chen and Paull, 2018; Faleiro, 2022; Mercado-Silva, 2018; Wakchaure et al., 2021). Vietnam, the largest exporter of dragon fruit, contributes to over 50% of the global production, with dragon fruit cultivation area in the country remarkably increasing from 5,512 hectares in 2000 to approximately 55,000 hectares in 2018 (Sakata, 2021). Nevertheless, dragon fruit production worldwide faces major challenges, including diseases that pose a significant threat leading to substantial reduction in crop yield (Balendres et al., 2019).

Dragon fruit canker (DFC), caused by Neoscytalidium dimidiatum (Penz.) Crous & Slippers, is the most destructive disease on dragon fruit (Hylocereus spp.) worldwide (EFSA, 2023; Espinoza-Lozano et al., 2023; Hong et al., 2020; Retana-Sánchez et al. 2019; Salunkhe et al. 2023; Serrato-Diaz et al. 2021). Extensive research conducted over the past decade in various countries, including Malaysia, Costa Rica, and the USA, has consistently identified DFC as the predominant disease affecting both the fruit and stems of dragon fruit. The incidence of DFC in these regions has varied, ranging from 40–100% (Hong et al., 2020; Mohd et al., 2013; Retana-Sánchez et al., 2019). Published data regarding dragon fruit losses due to DFC is limited. DFC can be highly destructive in specific climatic conditions with warm temperatures and high rainfall, potentially reducing market value by up to 60% (Hong et al., 2020; Sanahuja et al., 2016). Severe DFC outbreaks usually occur in the summer, when temperatures are high, ranging from 25 to 35°C (Hong et al., 2020).

DFC manifests with diverse symptoms, affecting fruit and stems (cladodes) of dragon fruit trees, typically as stem canker, brown spots, and fruit rot (Balendres et al., 2022; Hong et al., 2020; Lan et al., 2012). It has been observed that DFC symptom, lesion size, and distribution pattern are substantially influenced by tolerance of dragon fruit cultivar, the aggressiveness of the pathogen, prevailing climatic conditions, and ontogenetic resistance of the plant organ. Young developing stems are more susceptible to infection than fully matured stems (Fullerton et al., 2018). Initial symptoms on stems can be depressed chlorotic spots that progressively enlarge, turning from orange to reddish-brown over time, and often merge to form large brown lesions. These reddish-brown lesions often coalesce to form larger brown lesions, which may exhibit either dark brown, or water-soaked tissue with a surrounding yellow halo. Eventually, these lesions can dry out leading to perforations in the stems. Symptoms of fruits resemble those seen on stems (Fullerton et al., 2018; Hong et al., 2020).

As dragon fruit production expands worldwide (Lobo et al., 2013; Wakchaure et al., 2021), comprehensive studies on DFC epidemiology and control have become increasingly crucial. No dragon fruit varieties are currently known to be resistant or tolerant to DFC, necessitating effective disease control measures. Current DFC control depends on stem pruning, grove sanitation, and application of fungicides during critical periods. However, challenges arise in countries or regions where fungicides may not be registered, only a few fungicides are registered, or their number of applications are limited per season (CDMS, 2019; MAPA, 2022). For example, in South Florida, only a few fungicides are registered for dragon fruit, such as azoxystrobin (e.g., Abound, Aframe), fludioxonil (e.g., Scholar SC), and cyprodinil mixed with fludioxonil (e.g., Switch 62.5 WG) (CDMS, 2019). Based on the rates used, limited applications of the fungicides are allowed for growers to apply each year. For instance, applying Switch 62.5 WG at the highest rate is restricted to a maximum of four times per year.

Given the prevalence of DFC, it has become essential that studies are focused on addressing this issue by determining the effectiveness of cultural practices, the efficacy of novel fungicides, and screening variation of tolerance/resistance in dragon fruit cultivars. While some studies have examined chemical and biological fungicides against N. dimidiatum in controlled laboratory conditions (An et al., 2020; Intana et al., 2023; Taguiam et al., 2020), there is a need for further research conducted in field conditions. Regrettably, the absence of standardized disease assessment methods is currently impeding the efforts to mitigate the damage caused by DFC. Furthermore, this hampers the comparison of data from studies at different locations by researchers, compromising the reliability and comparability of the studies. A standard area diagram set (SADs), which estimates the percentage of diseased leaf tissue in relation to the whole tissue, would be an appropriate method for accurately assessing DFC severity.

This study aimed to develop and validate SADs to be used for accurate DFC severity assessment on dragon fruit and for the advancement of effective disease management strategies in dragon fruit production.

To develop the SADs, 121 stems (cladodes) of dragon fruit displaying varied DFC symptoms were collected from three distinct sites: two commercial plantations and one experimental plantation affiliated with UF/IFAS Tropical Research and Education Center (TREC), all located in Homestead, FL. To comprise the wide diversity of symptoms, the sampled stems were collected from different growth stages (mature and juvenile) and varieties (both white-flesh and red-flesh). The selected varieties included for white-flesh varieties: ‘Vietnamese’, ‘Alice’, ‘American Beauty’, ‘Lake Atitlan’, ‘David Bowie’ and red-flesh varieties: ‘Natural Mystic’, ‘Physical Graffiti’, ‘Halley Comet’, ‘Purple Haze’, ‘Voodoo Child’, and ‘Bloody Mary’. Digital images of the stems were captured with a digital camera and used to determine canker severity based on the percentage of affected leaf area using Quant v.1.0.1 software (Vale et al., 2003). Levels of disease severity were defined by considering the lowest and highest DFC observed in the field by natural infection. Given the wide variation in size, thickness, and curvature of the stems, a reference stem template was used to construct the disease diagrams. CorelDRAW Graphics Suite (2022) software were employed to incorporate lesions and their distribution in the designated template. To accurately capture the diversity of disease patterns observed in the field (e.g., lesion size and distribution), the SADs was composed using two versions. One version emphasized the presence of small flecks and spots, while the other incorporated predominantly the brown lesions and cankers. Each version encompassed a set of nine individual diagrams, with DFC severity intervals increasing linearly.

In the validation process, a dataset comprising 50 images exhibiting varying degrees of DFC severity was assembled and compiled into a Microsoft PowerPoint file. A group of 18 individuals with no prior experience in rating diseases severity were invited to this study. In the first step, the raters evaluated the DFC severity in each image without the use of the SADs. Subsequently, the same set of images were randomly presented in a different order, and the same raters reevaluated DFC severity using the SADs developed. Each rater estimated the DFC severity for each image presented within 20 seconds. A 10-minute break was provided between the two assessments (steps).

The accuracy (υ − scale bias; u − location bias; C_b − bias coefficient factor), precision (r − correlation coefficient), agreement (ρc − Lin’s concordance correlation coefficient) and inter-rater reliability (R² − coefficient of determination) of the estimates with and without the use of SADs were calculated as previously described (Dolinski et al., 2017). The statistical analyses were performed using R software (R Core Team, 2023). The Lin’s concordance correlation (LCCC) statistics were estimated by the epi.ccc function of the epiR package (Stevenson et al., 2023). The built-in boot. sample R function was used for the equivalence test. The ρ was estimated using the icc function of the irr R package (Gamer et al., 2022).

In this study, we developed a SADs to assess the severity of DFC symptoms based on the complexity, distribution, and diversity of symptoms. The SADs covered nine severity levels, ranging from 0.5–60% with a linear increase (Fig. 1).

Levels of DFC severity varied according to the area where the stems were collected in Homestead, FL. The DFC severity of the sampled stems ranged from 0.3–60.09%. However, DFC severity rarely exceeded 5% on the stems collected from conventional commercial groves due to the regular fungicide applications and sanitation adopted by growers in this area. Disease severity of less than 5% was found in 35.5% of the total stems collected (n = 43). The highest values of disease severity were observed in an experimental plantation located at the UF/IFAS Tropical Research and Education Center (TREC). DFC severity ranging from 5–20% was relatively common in this location, affecting 51% of the stems sampled (n = 42). This was primarily because fungicides were occasionally applied and pruning was rarely carried out for these experimental dragon fruit trees.

DFC manifested a diversity of symptoms in the stems collected, and the variations in the disease were noticed depending on the growth stage, variety, and location where the stems were collected. On the juvenile stems, DFC symptoms commonly manifested as numerous isolated chlorotic flecks (yellowish spots) and reddish-brown spots. As the severity exceeded 10%, these flecks and spots tended to coalesce, affecting a larger portion of the stem surface, and resulting in up to 60% of disease severity. Conversely, mature stems exhibited a different set of symptoms, including brown to grayish spots, necrotic lesions, cankers, dry tissues, and shoot holes. These symptoms varied in size, distribution, and density, depending on the varieties of the stems. These distinct symptom profiles led to the development of two versions of SADs in this study. One version focused on the presence of minute flecks and spots, while the other primarily incorporated necrotic lesions and cankers.

All assessments performed without and with the use of SADs resulted in linear relationships between estimated and actual disease severity of DFC (Fig. 2). The use of SADs significantly improved the accuracy and precision of DFC severity estimates by the raters on the dragon fruit stems. The statistical parameters (u, υ, C_b, r, and ρc) of Lin’s concordance correlation (LCCC) were significantly improved when the raters used the SADs to estimate the DFC disease severity. The statistical parameters values were: location bias - u (no SADs = 0.554, with SADs = -0.051) (confidence intervals - CI = -0.772 - -0.439), scale bias - υ (no SADs = 1.447, with SADs = 1.028) (CI = -0.533 - -0.304), bias coefficient factor - C_b (no SADs = 0.791, with SADs = 0.982) (CI = 0.141–0.239), correlation coefficient - r (no SADs = 0.884, with SADs = 0.918) (CI = 0.010–0.057), and Lin’s concordance correlation coefficient - ρc (no SADs = 0.702, with SADs = 0.902) (CI = 0.146–0.252). As the CI did not embrace zero, the difference was significant (α = 0.05). The inter-rater reliability of assessments by the 18 raters was also significantly improved. The mean of the inter-rater coefficient of determination (R²) of the pairwise comparisons was 0.749 (minimum = 0.471, maximum = 0.925) and 0.810 (minimum = 0.635, maximum = 0.931) without and with SADs, respectively. The 95% confidence interval (CI) of this mean was 0.041 to 0.081. As the CI did not embrace zero, the difference was significant (α = 0.05).

The improved precision of DFC severity assessment using the SADs was also confirmed by a significant reduction in absolute error. Without the use of SADs, evaluators had errors greater than 20% for 27.2% of estimates (n = 900) with errors reaching 55.8%. However, when SADs were used, only 3% of severity estimates exceeded 20%, and the maximum observed error was 27.2%. Most raters tended to overestimate disease severity without the use of SADs. The tendency to overestimate DFC severity was reduced using the SADs, although there was still potential for underestimation. This trend was consistently observed among raters, as most estimates with SADs yielded negative absolute errors. Still, the use of SADs resulted in an overall reduction of absolute error (Fig. 3). Various factors, such as lesion shape, size, density, and distribution, can influence disease severity assessment (Bock et al. 2022). Depending on the specific pathosystems, studies on SADs may lead to both underestimations (Duarte et al. 2013; Gomes et al. 2004) and overestimations (Duan et al. 2015; Domiciano et al. 2014) of disease severity.

Infected stems in the early season serve as a source of inoculum for N. dimidiatum, affecting flower buds and/or developing fruits during the growing season (Hong et al., 2020). Even with low levels of severity on stems, the incidence of fruit canker can potentially reach 100% in commercial groves (data not shown). To comprehensively understand the detrimental effect of DFC on fruit quality and yield, developing SADs to measure fruit severity in future studies is also essential. Hence, it is crucial to monitor the disease and establish appropriate and effective management programs in the early stages of dragon fruit production in order to prevent or minimize further disease impacts on the fruits. In this study, we developed and validated a SAD set for DFC severity, which represents a significant step towards more effective disease control in dragon fruit cultivation. The SADs presented various symptom patterns, making it a versatile tool for assessing DFC severity in different varieties of dragon fruit plants. Implementing this tool will help address the current issue of lacking standardized DFC assessment methods, ensuring precise and accurate disease evaluation across various research studies and locations.

Conflict of interest

All authors declare that they have no conflicts of interest.

Acknowledgements

We extend our gratitude to Allysson Arianna Plaza for her invaluable support throughout this study, and we appreciate the dedication of all the volunteers who took part in the validation process. The author HSSD would like to thank the National Council for Technological and Scientific Development (CNPq/Brazil) for the research scholarship. The work upon which this publication is based was funded, in whole or in part, through a subrecipient grant awarded by the United States Department of Agriculture, Agriculture Marketing Service through the Florida Department of Agriculture and Consumer Services Specialty Crop Block Grant Program (AWD11679; 2022–2024). The contents do not necessarily reflect the views or policies of the United States Department of Agriculture nor does mention of trade names, commercial productions, services, or organization imply endorsement by the U.S. Government.

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A Standard Area Diagram Set for Assessing Dragon Fruit (Hylocerus Spp.) Stem Canker Severity Caused by Neoscytalidium Dimidiatum

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