Analysis of Spatio-Temporal Distribution and Agro-ecological Factors Influencing Carrot Leaf Blight (Alternaria dauci) in East Hararghe, Ethiopia
Article information
Abstract
Carrot (Daucus carota L.) is a popular vegetable crop of nutritional and economic importance worldwide, including in Ethiopia. However, the productivity of the crop is constrained by carrot leaf blight (CLB) caused by Alternaria dauci. Field surveys were conducted during the 2020 and 2021 cropping seasons to assess the distribution and intensity of CLB and to determine its association with agro-ecological factors in East Hararghe, Ethiopia. A total of 170 carrot fields were inspected from three major carrot-growing (Haramaya, Kersa, and Kombolcha) districts of East Hararghe Zone, Ethiopia. Association of the disease incidence and severity with agro-ecological factors were analyzed using a logistic regression model. Out of 170 fields assessed over the 2 years, 98% of the fields were affected by CLB. From the field survey districts, Kersa had the highest mean disease incidence (63.2%) and severity (51.9%), while Haramaya district had the lowest disease incidence (41.6%) and severity (36.2%). Planting carrot in April, circulating farm-saved seed, poor crop residue management, sole cropping, fields that were adjacent to nearby carrot fields, unfertilized fields, and high weed density had significant association with higher CLB incidence (≥50%) and severity (≥35%) in the 2 survey years. In contrast, planting carrot in August, crop residue burial, planting commercial seeds, intercropping, planting carrot away from other carrot fields, crop rotation, soil fertilization, and good weed management were significantly associated with lower CLB intensity, which could be recommended as vital components for designing integrated management strategies against the disease and sustaining carrot production and productivity.
Introduction
Carrot (Daucus carota L.) is one of the most widely grown and regularly used cooking and raw vegetables in many households across the world (Paciulli et al., 2016). Carrot is popular for its richness in carotenoids, which are building blocks of vitamin A, and is also a good source of anthocyanins, dietary fiber, other vitamins, and antioxidants, which help in preventing many diseases (Arscott and Tanumihardjo, 2010). Other than its nutritional importance, carrot has also a significant role in the national and global economy as a source of income for smallholder farmers as well as large-scale commercial carrot root growers. According to the reports of the Food and Agriculture Organization (Food and Agriculture Organization/Statistical Database, 2022), China produced 21.48 million tons of carrots and turnips on 415,656 ha of land in 2021, making it the world's largest producer and exporter. Uzbekistan was the second largest producer and exporter of carrots and turnips, producing 2,769,613 tons on 38,922 ha of land, followed by the United States of America with a production of 2,259,000 tons on 32,210 ha of land in the same 2021 cropping year (Food and Agriculture Organization/Statistical Database, 2022).
In Ethiopia, carrot is produced in different agro-ecologies from mid to high altitudes during the main cropping season and the dry season using irrigation schemes and its production has increased as a result of increased urbanization and awareness about carrot as an income and nutrition source (Tabor and Yesuf, 2012). During the 2021/2022 main cropping season, about 31,671.6 tons of carrot was produced on 6,759.92 ha of land in the country (Central Statistical Agency of Ethiopia, 2022). Haramaya and Kombolcha districts of the East Hararghe zone are among the potential vegetable-producing areas of eastern Ethiopia with a concentrated small-scale production and a considerable contribution to the national economy through the export of carrot and other vegetables to the neighboring countries, i.e., Djibouti and Somalia (Tegegn, 2013). In 2021, Ethiopia earned USD 8,481,000 in revenue from the export of 42,292.39 tons of carrot (Food and Agriculture Organization/Statistical Database, 2022).
Even though the production of carrot has been increasing due to increased area coverage, the average yield (4 t ha-1) of carrot per unit area is much lower than the world's average, which was 38 t ha-1 during 2021 (Food and Agriculture Organization/Statistical Database, 2022). The low productivity of the crop could be associated with several production constraining factors, such as unavailability of high-quality carrot seeds, lack of improved production practices, and plant diseases and insect pests (Emana et al., 2015). Carrot diseases, such as root-knot nematode (Meloidogyne spp.), carrot leaf blight (CLB) caused by Alternaria dauci, and powdery mildew (Oidium spp.) were reported as major diseases in East Hararghe Zone, Ethiopia (Hussien, 2006). Among the carrot production constraining diseases, CLB is one of the most widely distributed and destructive foliar diseases of carrot in almost all carrot-producing regions of the world (Dugdale et al., 2000; Farrar et al., 2004; Khalmuminova et al., 2020; Liu et al., 2023; Pryor et al., 2002).
CLB is a polycyclic disease and common problem in carrot-production areas with high humidity, moderate temperature, and frequent rainfall, and areas that practice dew or sprinkler irrigation during the growing seasons (Davis, 2004; Farrar et al., 2004). Typical symptoms of the disease include dark-brown-to-black spots on older leaves, and the disease can cause rapid blight of carrot leaves and reduce photosynthetic area, resulting in poor growth (Souza et al., 2001). The pathogen infects inflorescence, seeds, and developing seed-lings (Pryor et al., 2002). Severe CLB epidemics weaken or destroy leaves and petioles, leading to harvesting difficulties, reduced carrot root size, and causing 40‒60% yield loss (Ben-Noon et al., 2001; Davis, 2004). Alternaria species persist in infected seeds and crop residues with high survival and distribution potential, and the pathogen is often disseminated through infested and infected carrot seeds (Lima et al., 2016). Thus, infected seeds and crop residues serve as a primary source of inoculum for the rapid spread of the disease in the field (Soteros, 1979).
In Ethiopia, the occurrence of CLB with considerable damage in Shewa areas dated back to 1979 as reported by Kidane (1993). CLB incidences ranging from 28% to 81% were reported in a field experiment conducted in East Hararghe more than a decade back (Mengistu and Yamoah, 2010). In addition, an experiment conducted to develop methods of quality carrot seed production at Haramaya University indicated a high percentage of carrot seed infection by A. dauci, which reached up to 100% (Debasso, 2018).
Despite these reports on the occurrence of the disease, studies regarding the distribution and intensity of CLB disease in major carrot-producing areas of Ethiopia remained scanty. On the other hand, a comprehensive assessment of CLB disease and identifying the factors that influence disease incidence and severity are essential to develop effective CLB management strategies for sustainable production and productivity of carrot. Therefore, the study was carried out with the objectives to: 1) assess the distribution and intensity of CLB disease in major carrot-growing areas and 2) determine the association of CLB incidence and severity with major agro-ecological factors in East Hararghe Zone, Ethiopia.
Materials and Methods
Description of the survey areas.
Field surveys of CLB disease were conducted in three major carrot-growing districts (Haramaya, Kersa, and Kombolcha) of East Hararghe, Ethiopia, during the 2020 and 2021 main cropping seasons. The field survey areas are located between 09° and 10° N latitude and 41° and 42° E longitude at an altitude that ranges from 1,921 to 2,191 meters above sea level (m.a.s.l.). The geographical locations of the survey districts are illustrated in Fig. 1. Temperature, rainfall, and relative humidity data of the survey districts were obtained from the National Meteorological Station, JigJiga Branch of Ethiopia, and shown in Fig. 2.
Map showing the surveyed districts for carrot leaf blight disease in East Hararghe, Ethiopia during the 2020 and 2021 cropping seasons.
Total monthly rainfall (RF) and mean minimum (Tmin) and maximum temperatures (Tmax) and relative humidity (RH) of the survey districts of East Hararghe, Ethiopia, during the 2020 and 2021 main cropping seasons.
Sampling procedures.
The field surveys were conducted in the three major carrot-growing districts, namely Haramaya, Kersa and Kombolcha of East Hararghe, Ethiopia, during October 2020 and 2021 main cropping seasons. The districts were purposely selected based on their potential for carrot production. During the survey periods, discussions or consultations were made with district officers and the extension (advisory) staff, who closely work with farmers, of each respective district agriculture office to identify potential carrot-production areas and to have an understanding of carrot production and the challenges associated with carrot production across the districts and farmers’ associations (FAs). Accordingly, seven potential carrot producing FAs from Haramaya district and five FAs each from Kersa, and Kombolcha districts were purposely selected based on their intensity of carrot production, and a total of 17 FAs were considered from the three districts. To assess the disease prevalence, incidence, and severity of CLB and to determine the factors that are associated with and affecting CLB disease incidence and severity across the selected carrot producing districts and FAs, five carrot fields per FA were inspected each year and, thus, 10 carrot fields were assessed from each FA over the two cropping years. Random sampling was used to select carrot fields at each FA at a distance of 3–5 km intervals towards the main and feeder roads and a total of 170 fields were assessed over the 2 years. A systematic sampling approach was also followed to assess the disease intensity in each field.
Disease assessment.
Disease assessment was carried out in each field along two diagonals (X-shape transect) using a 1 m2 quadrat. Five quadrats were sampled at 5‒10 m distance between sampling points at each field, and the carrot plants in each quadrat were considered as sampling units. Disease prevalence was determined by visually inspecting the fields for the presence or absence of the disease and expressed as percentages using the formula:
To assess disease incidence, the number of plants showing CLB symptoms per quadrat were counted and expressed as percentages of the total number of carrot plants per quadrat using the following formula:
In each quadrat, disease severity was scored from 10 randomly taken carrot plants based on typical CLB symptoms (dark-brown-to-black spots on the leaves) using a rating scale of 1 to 9, where 1=0% (healthy), 2=1% blighted, 3=2‒5% blighted, 4=6‒10% blighted, 5=11‒20% blighted, 6=21‒30% blighted, 7=31‒40% blighted, 8=41‒50% blighted, and 9=more than 50% of the leaf surface is blighted as described by Gugino et al. (2007). Disease severity scores were converted into a percentage severity index (PSI) for analysis with a formula suggested by Wheeler (1969):
During the field survey, representative samples of the symptomatic carrot leaves were collected and taken to Plant Pathology Laboratory of Haramaya University, Ethiopia, for pathogen analysis to confirm the identity of the target disease. Altitudes and geographical coordinates of each inspected field were recorded with a global positioning system device. Data on the factors that might influence the disease, such as seed source, sowing date, fertilizer application, carrot variety planted, field preparation, preceding crops, and residue management, were collected with face to face interviews with the farmers who own the sample fields, and interviews were held in the local language, ‘Afaan Oromo’, with questionnaires. The growers were directly consulted on the spot to obtain the required information during the field survey periods. Other factors, including carrot growth stage, cropping system, planting pattern, type of weed, and nearby crops, were assessed by direct visual observation of the fields, and the number of carrot plants and weeds was counted to determine carrot and weed densities per 1 m2 quadrat at each sampling point.
Data analyses.
The disease prevalence, incidence, and severity data were summarized with descriptive statistics. The association of the agro-ecological factors with disease incidence and severity were analyzed using a binomial logistic regression model with the SAS PROC GENMOD procedure (Statistical Analysis System, 2016). The GENMOD procedure is a statistical analysis procedure in SAS software that enables to perform a logistic regression analysis for various types of response variables, including count data and binary outcomes (Statistical Analysis System, 2016). Disease incidence and severity data were categorized into distinct groups of binomial qualitative data for the association analysis (Yuen, 2006). According to Bolkan and Reinert (1994), a disease severity value of 35% is the threshold to apply the first fungicide spray for CLB disease. Thus, 35% was picked as a cutoff point, and class boundaries of <35% and ≥35% were selected for disease severity data. Moreover, the mean disease incidence of the overall assessed fields (50%) was picked as a cutoff point. Class boundaries of <50% and ≥50% were set for disease incidence to get binary dependent variables for CLB. Based on the categorization of the disease incidence and severity data, a contingency table was made to show the bivariate distribution of independent variables, incidence, and severity of the fields (Table 1). The mean disease incidence and severity of the variables and variable classes were also summarized in Table 1. In the logistic regression analysis, the association of the agro-ecological factors (independent variables) with CLB incidence and severity was tested twice. First, in a single-variable model (type 1 analysis), and second, when entered last into the model with all other independent variables (type 3 analysis). The single-variable model examines the association of each independent variable with the outcome, in our case the incidence and severity of CLB. Whereas the multiple variable model examines the simultaneous effects of the factors on the outcome. The variables that were significantly associated with disease incidence and severity when entered first and last into the model were added to a reduced multiple-variable model to determine how individual classes within categorical variables influence the response variables, incidence and severity (Yuen, 2006). In a reduced multiple-variable model, analysis of the deviance reduction (DR) was carried out for each variable and the deviance, the logarithm of the ratio of two likelihoods, was used to compare the single and multiple variable models. Analysis of the DR between the likelihood ratio tests (LRT) was tested against a chi-squared distribution to evaluate the significance of the independent variables (McCullagh and Nelder, 1989). The reduced multiple-variable model in the GENMOD procedure provides parameter estimates and their standard errors for each class of categorical variables (Yuen, 2006). The parameter estimate (the natural logarithm of the odds ratio) in the logistic regression model indicates how independent variables/factors influence the likelihood of log-odds of a binary response. If the probability of the outcome is denoted as (P), the logistic regression model assumes that the logarithm of the odds of P (P/(1-P)), which equals logit (P), is a linear function of the independent variables (Yuen et al., 1996). In this case, the outcomes were the probability that CLB incidence exceeds 50% and severity exceeds 35% in a given carrot field. Different agro ecological factors considered in the analysis were the independent variables. The odds ratio was calculated by exponentiation of the parameter estimates and used to compare the effect of variable classes based on a reference point. The odds ratio in this case is the likelihood of disease incidence and severity exceeding 50% and 35% when a field was exposed to a given class of categorical variable compared to the reference class of the variable. This type of analysis has been used to study various epidemiological factors related to the incidence and severity of plant diseases. It was used to determine the association of bean rust and common bacterial blight epidemics with cropping systems (Fininsa and Yuen 2001), to assess factors influencing disease epidemics of chocolate spot (Botrytis fabae) of fababean (Sahile et al., 2008), agro-ecological factors influencing geographic distribution and epidemic development of hot pepper wilt complex (Alehegn et al., 2022), association of wheat Fusarium head blight with biophysical factors (Getahun et al., 2022), and the intensity of Ascochyta blight of chickpea with cropping systems and cultivation practices (Addisu et al., 2023).
Contingency table and mean (mean±SE) CLB disease incidence and severity for different independent variables used in the logistic regression analyses of the distribution of carrot leaf blight (Alternaria dauci) in three survey districts (n=170) of East Hararghe, Ethiopia, during the 2020 and 2021 main cropping seasons
Moreover, the t-test was run for the disease severity data for the variables that had two variable classes to determine the statistical difference in the mean disease severity of each variable class (Table 2).
t-test analysis of mean severity of CLB disease in East Hararghe, Ethiopia, during the 2020 and 2021 main cropping seasons
Results
General features of the survey fields.
The survey carrot fields were located at altitudes ranging from 1,921 in Kersa district to 2,191 m a.s.l. in Kombolcha district. Most (73.5%) of the inspected fields were located at an altitude ≥2,000 m.a.s.l., and the rest of the fields (26.5%) were found below an altitudinal range of 2,000 m.a.s.l. As indicated in the contingency table (Table 1) of the agro-ecological factors (the variables and variable classes), most of the farmers used to grow Nantes (41.8%) and local (48.2%) carrot varieties, and only 10% of the farmers’ fields were planted with Chantenay carrot variety. The carrot varieties were grown either in sole (70%) or intercropping systems (30%). The component crops in the intercropping system were mainly khat (Catha edulis) and a few fields with maize (Zea mays). Planting dates varied from April to August. In the study areas, 66.5% of the carrot fields, which were planted for the production of carrot roots, were at the vegetative growth stage at the time of assessment. The remaining 33.5% of the carrot fields were at the flowering growth stage which were primarily planted for carrot root production and were left on the fields for seed production purpose after uprooting most of the carrot roots. About 43.5% of the farmers’ fields were fertilized using urea and nitrogen, phosphorus, and sulfur (NPS)-blended fertilizers. Crop rotation was commonly practiced for 60% of the carrot fields and most (52.4%) of the farmers noted to remove or bury crop residues before planting. Regarding crops grown before carrot, shallot, carrot, beet root, and cabbage were the commonly cultivated preceding crops. The commonest crops cultivated near to inspected carrot fields during the survey were maize, khat, carrot, and other vegetables, such as beet root, parsley, shallot, and lettuce (Table 1).
Hand weeding was usually practiced by farmers to remove weeds from their fields. Despite the attempts to contain the weeds, different levels of weed density were recorded during the field survey periods. Hence, about 28.8% of the carrot fields were well managed (0–10 weeds m-2), while 31.8% of them were moderately (11–20 weeds m-2) infested by weeds, and the remaining 39.4% of the carrot fields were poorly managed and had high (≥20 weeds m-2) weed density (Table 1). The predominantly observed weeds across the survey areas were Bidens pilosa (blackjack), Cyperus rotundus (brown nutsedge), Sonchus asper (spiny sowthistle), S. oleraceus (common sowthistle), and Tagetes minuta (marigold). Regarding field preparation, 54.7% of the carrot fields were flat lands, while the rest 45.3% were prepared as broad beds and planted in rows (>70%) or the rest of the fields in broadcasting patterns. Among the fields considered in this assessment, 66.5% of them had 70 to 90 plants m-2 and the rest, 33.5% of the fields contained ≥90 plants m-2. About 58.2% of fields were planted with commercial seeds, and 41.8% of the farmers used to circulate their farm-saved seeds collected from previous harvests (Table 1). It was also noticed that CLB was prevalent in almost all of the fields (98%) inspected and the farmers used local names to call the disease, as ‘wag’ in Amharic or ‘ Waagii’ in Afaan Oromo language.
During the field survey, galls of root-knot nematodes (Meloidogyne spp.) were observed on uprooted carrots in the fields of the three districts, and root rot (Sclerotinia root rot, caused by Sclerotinia sclerotiorum) was observed on carrot plants that were nearly at seed maturity in a few fields from only Haramaya district.
Distribution and prevalence of CLB.
The disease was highly distributed in all the survey districts with high prevalence. During 2020, CLB prevalence of 100% was recorded from Kersa and Kombolcha districts, followed by Haramaya district, which recorded 91.4% of disease prevalence. In 2021, a CLB prevalence of 100% was noticed across all three districts with varying levels of disease incidence and severity.
Incidence and Severity of CLB.
The mean and standard errors of disease incidence and severity of the surveyed districts and other agro-ecological factors considered in this study are shown in Table 1. Among the districts, Kersa district was highly affected by the CLB disease with a 63.2% mean incidence and 51.9% severity, while Haramaya district had the lowest CLB incidence (41.6%) and severity (36.2%) in the 2 survey years. The disease incidence (37.9%) and severity (30.8%) of CLB were lower in fields located at an altitudinal range below 2,000 m.a.s.l., and higher disease incidence (56.2%) and severity (45.8%) were assessed from fields located at altitudes ≥2,000 m.a.s.l. Fields planted with the local carrot variety exhibited higher disease incidence and severity than fields planted with improved or commercial (Nantes and Chantenay) carrot varieties. With regard to planted date, the highest disease incidence (58.9%) and severity (50.1%) were assessed in carrot fields planted during May, while the lowest disease incidence (41.3%) and severity (33.8%) were recorded from fields planted during August. Detectable variations in disease components were also observed as far as seed source is concerned and lower disease incidence and severity were recorded from fields planted with commercial (imported) seeds than from fields planted with farm saved seeds (Table 1).
Regarding fertilizer application, the disease incidence and severity recorded in unfertilized fields exceeded by 16.7% and 13.8%, respectively, over the fields fertilized with urea and NPS blended fertilizers. Crop rotation was an important farmers’ practice influencing disease epidemics, and lower disease incidence of 41.6% and severity of 33.9% were recorded from fields that employed crop rotation than non-rotated fields with other crops (Table 1). Crop residue burying or removal practices reduced the disease incidence and severity by 22.5% and 17.7%, respectively, compared to fields with crop residues (Table 1).
Cropping systems were found to influence CLB intensity across the study areas in the 2 cropping years. In this regard, the sole-cropped carrot fields exhibited higher disease incidence and severity than fields with carrot intercropped with khat and maize, which reduced disease incidence by 24.7% and disease severity by 19.9% over sole cropping system. Carrot fields with high weed density were severely affected by CLB disease, in which the highest incidence (55.7%) and severity (47%) were assessed in high (≥20%) weed infested fields than in fields with low to medium (<20%) weed infestation (Table 1). Crop growth stage played a key role in the epidemic development of CLB (Fig. 3). For instance, carrot fields at the flowering growth stage had higher (67.1%) disease incidence while vegetative growth stage showed lower (42%) disease incidence. Higher (56.7%) mean disease severity was also recorded from carrot plants of flowering stage while lower (34.3%) severity was from carrot plants of vegetative stage (Table 1). It was also noted that higher disease intensity was observed on sparsely populated fields that contained 70 to 90 carrot plants m-2 than densely populated fields with more than 90 carrot plants m-2 (Table 1).
Carrot leaf blight epidemic in assessed fields at vegetative and flowering growth stages of the crop. Disease-free carrot field at vegetative growth stage (A), Leaf blight infested field at vegetative (root) stage (B), highly infected carrot plants at flowering stage in poorly managed field that was left for seed production (C).
The t-test analysis of the mean disease severity of the agro-ecological factors revealed that mean disease severity differences of the variable classes were highly significant (P≤0.0001) for most of the variables, except for year (t-value=0.84 and P=0.403) (Table 2). Thus, the mean severity of CLB disease significantly varied between carrot fields located at altitude ranges below 2,000 and above 2,000 m.a.s.l., sole and intercropping systems, fertilized and unfertilized fields, vegetative and flowering growth stages, and fields planted with commercial and farm-saved carrot seeds. Significant variations were also detected between the mean CLB severity of variable classes of other factors, including crop rotation practices, residue management, field preparation, planting pattern, and plant density. However, no significant (P>0.05) variation was observed in CLB disease severity between the 2020 and 2021 cropping seasons (Table 2).
Association of agro-ecological factors with CLB incidence and severity.
Association of the agro-ecological factors with CLB incidence and severity are presented in Table 3. The result of the logistic regression analysis showed that the factors, including district, altitude, planting date, fertilizer application, crop rotation, residue management, cropping system, nearby crops, preceding crop, weed management, growth stage, and seed source, showed significant (P≤0.05) association with disease incidence and severity when evaluated first into a single variable model. Except for district and altitude, those variables retained their significant relationship with incidence and severity when evaluated last in the multiple-variable model. However, independent variables such as variety, field preparation, planting pattern, plant density, and year did not show significant association (P>0.05) with CLB incidence and severity in either the single or multiple variable models (Table 3).
Logistic regression model for carrot leaf blight (Alternaria dauci) incidence and severity, and likelihood ratio test on independent variables in East Hararghe, Ethiopia, during the 2020 and 2021 main cropping seasons
Among the independent variables, crop rotation (χ2=18.07 and 5.52, 1 df), preceding crop (χ2=11.89 and 12.77, 3 df), fertilizer application (χ2=11.71 and 5.83, 1 df), and planting date (χ2=11.23 and 8.74, 3 df) were the most important factors associated with CLB severity when entered first and last into the logistic regression models, respectively. A similar trend was also observed for disease incidence for the stated variables that influence disease severity (Table 3).
Relative effect of agro ecological factors associated with CLB incidence and severity.
The variables that had significant association with CLB disease incidence and severity were tested in a reduced multiple-variable model. The results of the analysis of deviance of the variables and variable classes to incidence and severity, their parameter estimates and standard errors, as well as the odds ratio for each variable class are displayed in Tables 4 and 5. The residual deviance from the deviance analysis shows how well the model explains the response variables, CLB incidence and severity, as the factors/variables were added to the model (Tables 4, 5). Lower residual deviance values indicate a better model fit. As the variables were added, the residual deviance decreased, suggesting the importance of the variables in explaining disease incidence and severity. For instance, in the deviance analysis of CLB incidence, the initial residual deviance of the model 227.99 (intercept) dropped to 195.89 when the variable planting date was added and further decreased to 91.81 (seed source) as more variables were included (Table 4). Similarly, the residual deviance from the deviance analysis for CLB severity showed a reduction from 221.93 (intercept) to 87.50 (seed source) as the variables planting date, fertilizer application, crop rotation, residue management, cropping system, nearby crops, weed density, growth stage, preceding crop, and seed source were sequentially added to the model (Table 5). The decreased residual deviance signifies reduced unexplained variability, confirming the importance of the factors in determining CLB incidence and severity. The DR results of the LRT that show the explained variability of the model due to each variable class with P-values/(Pr>χ2) values indicating statistical significance are displayed in Tables 4 and 5.
Analysis of deviance, natural logarithms of odds ratio and standard error of carrot leaf blight, CLB (Alternaria dauci) incidence and likelihood ratio test on independent variables in reduced regression model in East Hararghe Ethiopia, during the 2020 and 2021 main cropping seasons
Analysis of deviance, natural logarithms of odds ratio and standard error of carrot leaf blight, CLB (Alternaria dauci) severity, and likelihood ratio test on independent variables in reduced regression model in East Hararghe, Ethiopia, during the 2020 and 2021 main cropping seasons
The results of the odds ratio values of the variable classes of the factors in the reduced multiple-variable model revealed that planting carrot early in April to May had the highest probability of higher disease incidence ≥50% and severity ≥35%, followed by the fields planted during June and July over August planting. Compared to carrot fields planted in August, there were 13.1, 4.3, and 2.9 times greater probabilities of incidence ≥50% and 13.6, 5.4, and 1.8 times greater probabilities of severity ≥35% for fields planted in May/April, June, and July, respectively (Tables 4, 5).
Applying urea and NPS fertilizers had a lower probability of disease incidence exceeding 50% and severity exceeding 35%, while unfertilized fields had 12.8 and 5.6 times higher probabilities of occurrence of higher disease incidence and severity than the fertilized fields in that order. Nearby carrot crops had the highest probabilities of higher disease incidence ≥50% and severity ≥35%, which were about 10.1 and 20.5 times, respectively, over the fields neighbored by khat (Tables 4, 5).
Regarding weed density, the high likelihood of CLB disease incidence ≥50% and severity ≥35% were also associated with highly weed-populated fields, followed by moderately weed-populated fields compared with well managed carrot fields. In this regard, high weed density was associated with higher disease incidence with 9.5 times greater probabilities (Table 4) and with higher severity, with 10.9 times greater probabilities (Table 5) than low weed density. Moderate weed density was associated with higher disease incidence and severity with 8.3 and 8.9 times greater probabilities, respectively, than low weed density (Tables 4, 5). In addition, sole cropped carrot fields were associated with higher disease incidence with 4.5 times greater probability and severity with 8.3 times greater probability of disease risk than carrot fields intercropped with khat during the two cropping seasons. Conversely, applying crop rotation, proper removal of crop residues, and planting commercial (imported) carrot seeds were associated with lower (<50%) disease incidence and lower severity (<35%) than their respective counterparts. The vegetative growth stage also had a lower probability of high disease incidence and severity than at the flowering growth stage (Tables 4, 5).
Discussion
CLB was found prevalent in almost all the survey fields of East Hararghe, Ethiopia. Though there is a dearth of recent information regarding the status of the disease, Ashagari (1973) reported alternaria leaf blight of carrot as an economically important disease among vegetable diseases in Eastern Ethiopia. The distribution and high intensity of the disease across the inspected districts could be due to favorable weather conditions of the areas along with other agro-ecological factors that could encourage the initiation and development of disease epidemics. The survey districts experienced a rainy season from April to September with high levels of rainfall that reached 254 mm (in August), and mean monthly maximum temperatures ranged from 21.1 o C to 28.1 o C with moderate relative humidity (>40%) in most of the cropping months (Fig. 2). Alternaria leaf blight frequently occurs in humid carrot-growing areas with higher rainfall and moderate temperatures (Farrar et al., 2004). At temperature ranges of 16–28°C, Alternaria dauci infections occur within 8 to 12 hr, and the fungus easily sporulates on dead necrotic tissues, and the spores easily germinate in dew and water droplets (Strandberg, 1988). Rain splashing can easily spread the spores from plant to plant, promoting infection, and as little as 2 hr of leaf wetness can initiate the conidial germination of Alternaria spp. to cause infection (Fagodiya et al., 2022).
The findings of this current study showed that agro-ecological factors influenced the incidence and severity of CLB disease. Higher disease incidence (≥50%) and severity (≥35%) were significantly associated with early planting of carrots (April to May) and flowering growth stage. This could be explained by the fact that early planting exposes the field for an extended period to the disease and an increase in the susceptibility of the crop with age, along with the prevailing conducive weather conditions. During the survey periods, the carrot fields planted in April and May remained in the field for a relatively longer period than those planted in August and the farmers used to leave those carrot fields unharvested until flowering and producing seeds. Most of those fields were severely infected with CLB disease and highly infested by weeds. In this regard, Fagodiya et al. (2022) indicated that an extended period of growing season results in an extended amount of time available for reproduction and dissemination of a pathogen and, thus, increases the chance of disease epidemics. Moreover, the age of a plant is one of the host factors affecting disease epidemics, as it can affect the level of disease resistance and susceptibility to a disease. The age of the plant at the time of deposition of the pathogen from a certain source may affect pathogen penetration and the development of infection (Fininsa, 2022). Previous research findings of Soteros (1979) also noted that, as the age increases, the carrot leaves become more susceptible to A. dauci, implying that alternaria diseases primarily infect older leaves and senescing tissues, and the resistance of young carrot leaves to A. dauci was suggested to be related to their higher content of reducing sugars, tannin, and low nitrogen content (Pryor, 2002; Soteros, 1979).
In this study, it was identified that circulation of farm-saved seeds in each successive cropping season is common, and, hence, planting farm-saved carrot seeds increased disease incidence and severity by 25.6% and 21.7%, respectively, over commercial seeds. Regardless of the type of crops grown, the findings of different researchers confirmed that farm-saved seeds are compromised for being highly infected with fungal pathogens as compared to certified seeds (Bishaw et al., 2013; Dauda et al., 2017; Gyasi et al., 2020). Higher disease intensity recorded from fields planted with farm-saved carrot seeds might be associated with continuous uses of untreated farm-saved seeds that allow the introduction of the pathogen into the soil, increase the ease of buildup of inoculum of the pathogen, and cause disease epidemics in the field (Dauda et al., 2017; Gyasi et al., 2020). Alternaria spp. are the most frequently occurring seedborne fungi and A. dauci infected carrot seeds are major sources of primary inoculum for short- and long-distance dissemination of leaf blight disease (Zhang et al., 2020). Thus, planting relatively healthy seeds or fungicide-treated seeds is one of the primary measures that have been recommended for reducing the risks of disease development (Davis, 2004).
The findings of this present assessment showed that relatively lower disease intensity occurred on fertilized fields than on fields that did not receive fertilizers. This could be attributed to the impact of increased formation of new carrot leaves and delayed leaf senescence, maybe due to adequate nitrogen compared with unfertilized fields that were associated with higher CLB development. With regard to it, Westerveld et al. (2003, 2008) elucidated that even though the interaction between the CLB severity and nitrogen nutrition of the carrot crop is not clearly understood, higher nitrogen levels may increase the plant's vigor and delay maturation or leaf senescence, which consequently delays CLB development, resulting in less severe symptoms. Moreover, the findings of Westerveld et al. (2008) testified that increasing the rate of nitrogen would increase the number of live leaves per plant and decrease leaf senescence during the growing seasons.
Generally, plant nutrition is an important factor that can affect the response of plants to a disease. Nitrogen abundance in the soil increases the growth rates of plants and the production of young, succulent plant tissue and results in an extended vegetative phase. That is, adequate nutrition can enhance the plant's disease tolerance or resistance (Panth et al., 2020). However, low levels of soil nitrogen could reduce growth rate, weaken plants, and fasten aging, thereby making plants more susceptible to pathogens that primarily attack weak and slow-growing plants (Agrios, 2005). Weakened plant tissues, in relation to age, stress, or damage, are more prone to Alternaria infection than those tissues with good growth (Thomma, 2003). A fertilizer rate evaluation study under controlled and field conditions by Westerveld et al. (2003, 2008) showed that CLB severity and Cercospora leaf spot were reduced with increased application rates of fertilizers. In addition, Khatun et al. (2011) reported that application of NPK fertilizers reduced Alternaria leaf blight intensity on mustard.
Cropping systems influenced CLB epidemics in that higher disease incidence and severity were observed in sole carrot fields than those intercropped with khat. This might be explained from the perspective of the role of intercropping in plant disease management, as it has been known to provide better disease management when crops are intercropped with non-host plants (Sharaiha et al., 1989). According to a review made by Boudreau (2013), intercropping had reduced foliar fungal diseases in 73% of the reviewed phenomenological researches that compared diseases in monocrops and intercrops. For example, Narla et al. (2011) evaluated the effects of intercropping vegetables, such as carrot (Daucus carota), spider plant (Cleome hassleriana), and common bean (Phaseolus vulgaris), in the management of purple blotch (Alternaria porri) and downy mildew (Peronospora destructor) diseases of onion and demonstrated the benefits of intercrops in reducing the foliar diseases over the monocrops. Galande and Simon (2019) also noticed that intercropping of onion with common bean and chickpea (Cicer arietinum) reduced purple blotch (Alternaria porri) on onion. Therefore, intercropping carrots in khat fields could have reduced CLB disease, as khat plants may serve as a physical barrier or a trap for the spread of aerial moving spores. Furthermore, most khat growing farmers of East Hararghe commonly apply insecticides and other pesticides for the management of different insect pests and diseases of khat (Regassa and Regassa, 2018). Though it requires further analysis, pesticide drift upon khat spraying might have an effect on carrots intercropped within khat fields and might have contributed to the reduction of the intensity of CLB disease.
Weed density was an important factor that was significantly associated with the intensity of CLB. For instance, carrot fields with high weed density were heavily infected with CLB disease, with a mean disease incidence (55.7%) and severity (47.6%) in the two seasons. As it was reported for other pathosystems, weed infestation could promote the development of a disease through competition with the host for available resources that could reduce crops vigor for resistance and predispose them to diseases, and weeds modify the microclimate, such as enhancing relative humidity and leaf wetness, in a way that favors infection and disease development (Aragaw et al., 2019; Sahile et al., 2008). High relative humidity and periods of long leaf wetness are favorable conditions for infections to occur by the pathogen A. dauci (Farrar et al., 2004). Some other reports also revealed that weeds promote plant disease epidemics through harboring the pathogen and serving as an alternate host, and A. dauci was recovered from weed hosts, such as wild carrot and parsnip found in carrot fields, though carrot is a primary host for the pathogen (Pryor et al., 2002). Likewise, Lin et al. (2015) reported that A. dauci was found to cause leaf blight on Bidens pilosa and the weed has developed leaf spot symptoms after re-inoculation of the pathogen in China. Similarly, B. pilosa was a predominant weed species with leaf spot symptoms observed on the majority of the carrot fields during the current field survey periods. Thus, it is likely that the high weed infestation observed from the surveyed fields has contributed to the disease epidemics through harboring A. dauci growth, sporulation, and infection.
Crop rotation and residue management were among the cropping practices that significantly influenced the epidemics of CLB disease in both cropping seasons. It is customary that crop rotation can suppress a plant disease when applied for target pathogens that remain in the soil or on crop debris for only a few years (Panth et al., 2020). Unlike the pathogens that are soil inhabitants or saprophytes that survive in the soil for many years, A. dauci is a suitable pathogen to target for management with crop rotations, as it cannot survive for a longer period once the debris has decomposed. Pryor et al. (2002), who conducted an extensive study on the survival and persistence of A. dauci under different conditions, demonstrated that A. dauci can survive on infested leaf tissue that was left in fallow fields for up to a year. And hence, burying infected tissues in the soil affected the survival of the pathogen and declined A. dauci sporulation 5 months after burial of infected carrot leaf tissue in soil, and no sporulation was detected 8 months after burial (Pryor et al., 2002). In parallel to such findings, relatively lower disease intensities were observed on carrot fields where crop rotation and residue burial were applied in that the practices reduced the survival of the pathogen on infected crop residues and between carrot crops of the continuous production season in the current study.
Infested adjacent fields are documented to be ideal sources of inocula for several pathosystems. Similarly, during the current field assessment, higher incidence and severity were recorded from carrot fields planted adjacent to other carrot fields than from other fields covered with different crops. In agreement with the current findings, a study by Koike et al. (2017) reported that higher leaf spot severity was observed on lettuce and celery crops adjacent to carrot fields with severe Alternaria leaf blight, and A. dauci was recovered from those lettuce and celery crops with leaf spot symptoms. This might be due to the movement of airborne A. dauci spores between adjacent fields. Especially when production seasons overlap, conidia produced from mature fields serve as inoculum sources for recently planted neighboring fields (Farrar et al., 2004). Other reports as well indicated that significant numbers of spores of Alternaria species, such as A. solani, A. brassicicola, and A. alternata, were spread by wind to distances ranging from 6 to 20 m away from the sources of infections or inocula (Chen et al., 2003). In addition, the results of this study showed that fields neighbored by other vegetables, such as beetroot (Beta vulgaris), parsley (Petroselinum crispum), shallot (Allium ascalonicum; syn. Allium cepa var. aggregatum), and lettuce (Lactuca sativa), had higher probabilities of disease risk than carrot fields neighbored by khat, indicating that other vegetables could serve as alternate hosts for the pathogen/disease. However, further studies are required to confirm if those crops can alternatively host the pathogen.
The findings of the current study revealed that CLB was highly distributed in major carrot-producing districts of East Hararghe, Ethiopia. The logistic regression analyses showed that planting carrot in April to May, planting-farm saved seeds, poor residue management, sole cropping, flowering growth stage, fields neighbored by other carrot fields, lack of fertilizer application, and high weed density had a high probability of association with high disease incidence and severity. On the contrary, CLB incidence and severity were relatively low in planting commercial seeds, good residue management, at vegetative growth stage, in intercropped fields, and in fields with crop rotation practices, fertilizer received fields, and good weed management practices. Therefore, the present findings have profound implications for designing effective disease management strategies that integrate compatible options, such as planting improved or commercial seeds, residue burial, practicing crop rotation, intercropping, fertilizer application and good weed management, and planting carrots away from older carrot fields to suppress and/or prevent the disease; and such factors should be considered as year-round practices. However, as the disease is highly distributed in the survey areas and is economically important, only cropping practices are barely enough to adequately manage the disease. Therefore, chemical application/supplementation must be considered as an integral component of the integrated disease management strategy to reduce the epidemics of the disease. In addition, to reduce further spread of the pathogen through infected seeds, farmers need to be advised to plant physically or chemically treated seeds. Hence, future research should be carried out on the identification of the type, frequency, and concentration of seed treatment chemicals as well as fungicide sprays along with other cultural practices, to ensure CLB management and to sustain carrot production and productivity in the study areas and other locations with similar agro-ecologies.
Notes
Conflicts of Interest
No potential conflict of interest relevant to this article was reported.
Acknowledgments
The authors thank Ministry of Education, Dire Dawa University, and Carrot Aid for financial support of this research work. Haramaya University is also acknowledged for assisting and providing vehicle during the field surveys.