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Association of white rot (Sclerotium cepivorum) of garlic with environmental factors and cultural practices in the North Shewa highlands of Ethiopia
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Crop Protection 26 (2007) 1566–1573 www.elsevier.com/locate/cropro
Association of white rot (Sclerotium cepivorum) of garlic with environmental factors and cultural practices in the North Shewa highlands of Ethiopia Tamire Zewdea,, Chemeda Fininsaa, Parshotum K. Sakhujaa, Seid Ahmedb a
Department of Plant Sciences, Haramaya University, P.O. Box 138, Dire Dawa, Ethiopia b Ethiopian Institute of Agricultural Research, P.O. Box 2003, Addis Ababa, Ethiopia
Received 11 August 2006; received in revised form 15 January 2007; accepted 23 January 2007
Abstract Field surveys were conducted in North Shewa highlands, Amhara state, Ethiopia during 2003 and 2004 main cropping seasons to determine the distribution, prevalence and the association of garlic white rot (Sclerotium cepivorum) incidence with environmental factors and cultural practices. In both years a total of 385 garlic fields were surveyed in four districts, and 96.6% of the fields were infested with white rot. Disease incidence varied among districts and between years, altitude range, soil type and field management practices. The mean disease incidence in 2 years ranged from 21% in Lalo Mama Mider to 42% in Basona and Werena district, where it was significantly higher. The incidence in 2004 cropping season was higher by 37.28% than in 2003. Logistic regression was used to analyse the association of white rot incidence with environmental factors and cultural practices as independent variables. District, cropping year, soil type and weed management practices were significantly associated with white rot incidence in a multiple variable model. Higher incidence of white rot was significantly associated with Basona and Werena district. Lower incidences had a high probability of association with Angolela and Asagirt and Lalo Mama Mider (2003) cropping year and good weed management practices. In a reduced multiple variable model, year and weed management practice were significantly associated with lower white rot incidence. In garlic intercropped with Brassica there was very low disease incidence. The survey revealed high occurrence and distribution of white rot in the study area and effective and feasible management options need to be developed. r 2007 Elsevier Ltd. All rights reserved. Keywords: Abiotic factors; Allium sativum; Garlic; Sclerotium cepivorum; White rot
1. Introduction Garlic (Allium sativum L.) is one of the most important vegetable crops widely grown for use as a flavouring condiment in foods in different parts of the world (Tindall, 1983). Garlic is the second most widely cultivated Allium species in Ethiopia after onion (A. cepa L.). Ambo, Debre Work, Adet, Sinana, and other areas of the Ethiopian highlands produce the bulk of garlic (Getachew and Asfaw, 2000). In North Shewa highlands, garlic and onion are cultivated using rain supplemented by irrigation. However, Corresponding author. Tel.: +251 025 661 07 20; fax: +251 025 661 07 13. E-mail address: [email protected] (T. Zewde).
0261-2194/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2007.01.007
production of garlic is constrained by several biotic and abiotic constraints. Among the biotic constraints, fungal diseases are a major factor affecting production and productivity as well as the quality of garlic in different parts of the country. Among the fungal diseases, rust caused by Puccinia allii and white rot caused by Sclerotium cepivorum Berk. (Coley-Smith, 1987) and neck rot caused by Botrytis allii, B. squamosa and B. cinerea (Dennis, 1986) are the most important ones worldwide including Ethiopia. S. cepivorum produces no functional spores. Instead, it propagates only by the production of circular sclerotia (around 300 mm in diameter) which are produced on roots of decayed host plants (Coley-Smith and King, 1969). The sclerotia germinate and produce mycelium only in response to the presence of Allium root exudates (Coley-Smith and
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Holt, 1966). The germinated mycelia penetrate the root epidermis and invade the cortical parenchyma causing extensive tissue disintegration (Abd-El-Razik et al., 1973). Sclerotia spread in mass through movement of soil, water and in infested plant parts. Once introduced into an area, S. cepivorum is gradually spread by contaminated equipments and planting materials, and slowly the production of garlic in the entire field is threatened. White rot causes important economic losses in garlic production worldwide. In UK, 10% losses (Entwistle, 1990); and in Mexico (Andrea et al., 1996) and Brazil (Pinto et al., 2000) losses up 100% were reported. The disease is also serious in Canada and incidence can exceed 65% in commercial fields (Earnshaw et al., 2000). In Ethiopia, Mengistu and Seid (1993) reported heavy damage to garlic due to white rot. In recent years, white rot has become very important in major production areas of garlic (Mengistu, 1994). The yield loss due it has been found to range between 20.7% and 53.4% (Tamire et al., unpublished data). In Ethiopia, information on the distribution and importance of white rot has not been systematically analysed in major growing areas of the country. As white rot disease has become a recurrent problem in major garlic production areas of the country, information obtained from survey work is important for planning management strategies. Therefore, this study was conducted with objectives to determine the (i) incidence and prevalence of white rot in major growing districts, and (ii) its association with environmental factors and cultural practices.
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Amhara Regional state
Tarmaber
Lalo Mama Mider
Baso & Werena
Angolela & Asagirt
Fig. 1. Map of Ethiopia and the survey districts in the Amhara Regional State.
conducted from 25 September to 15 October in 2003 and 30 September to 20 October in 2004. Over 2 years, a total of 385 garlic fields were surveyed of which 25.9% were in Basona and Werena, 25.9% in Lalo Mama Mider, 24.9% in Tarmaber, and 23.1% in Angolela and Asagirt. In both years white rot was assessed at bulb formation stage (at about 120 d after planting). The areas surveyed and the geographic locations are indicated in Fig. 1.
2. Materials and methods
2.2. Survey methods
2.1. Survey sites
The survey was conducted by inspecting garlic fields, and interviewing growers in the districts. Fields were selected at random from each of the districts at intervals of 5 km along main and feeder roads. In each sample field, three quadrants (1 m 1 m) 5 m apart were sampled by making diagonal moves in the field. The plants in each quadrant were taken as the sample unit. The plant population in each quadrant was counted and the mean plant population density was obtained by averaging the plant population in the three quadrants. Incidence of white rot was assessed by counting the number of plants showing white rot symptoms (such as yellowing, discoloration, bulb rotting, and presence of mycelium and/or sclerotia around the base of the plant) in each quadrant and averages were taken for each field. During the survey, altitude (m), type of soil (vertisol or black soil and light soil), cropping pattern (row or broadcast planting), weed management practices and plant density were recorded for each sampled field. Growers were asked information on cropping system, cultivar, and cultural practices (time of planting, land preparation, previous crop, and disease control practices) employed.
White rot disease surveys in major areas of garlic production in the North Shewa highlands were conducted in four districts (Basona and Werena, Lalo Mama Mider, Tarmaber, and Angolela and Asagirt) of North Shewa highlands in 2003 and 2004 during the main rainy season. The survey districts differed mainly in altitude, weather and soil characteristics (Table 1). The survey was
Table 1 Characteristic features of surveyed garlic fields in four districts of North Shewa highlands, Ethiopia District
Altitude (m)
Annual total rainfall (mm)
Temperature (1C)
Soil type
Angolela and Asagrit Basona and Werena Lalo Mama Mider Tarmaber
600–2750
121–921
5–21.1
Light soil
1545–2960
695–905
6–19.7
Vertisol
1450–2960
725–842
7–17.9
Light soil
1900–3250
800–943
3–15.5
Light soil
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2.3. Data analysis Descriptive analysis was performed on all data collected from each field. In addition, data analysis was conducted to describe the distribution, prevalence and association of white rot incidence in relation to the independent variables listed in Table 2. Where significant difference for disease incidence existed, the mean disease difference were separated using the T-test at Po0:05. In the second analysis, the independent variables and variables class were categorized based on the frequency of fields (Table 2). Disease incidence (the response variable) was classified into a distinct class of bivariate qualitative data using the statistical analysis for science (SAS) procedure (SAS Institute, 2003) of the univariate procedure of disease
incidence as variables. Selected class boundaries were p30% and 430%. Tables of independent and variable classes for disease incidence were constructed to represent the bivariate distribution of the fields. The value corresponding to each independent variable represents the frequency of fields falling in the disease range (Table 3). The association of white rot incidence with the independent variables and variables class were analysed using a logistic regression model with the SAS procedure of the GENMOD procedure (SAS Institute, 2003). The GENMOD procedure estimates the parameters of the model numerically through an iterative fitting process. The GENMOD procedure fits a generalized linear model to the data by maximum likelihood estimation of the parameter. The logistic regression model allows the
Table 2 Categorization of variables used in analysis of distribution of white rot (Sclerotium cepivorum) incidence in four districts of North Shewa highlands, Ethiopia (n ¼ 385)
Table 3 Independent variable by disease contingency table for logistic regression analysis of garlic white rot (Sclerotium cepivorum) during 2003 and 2004 at North Shewa highlands, Ethiopia
Variable
Variable class
Number of fields
Independent variable
District
Angolela and Asagirt Basona and Werena Lalo Mama Mider Tarmaber 2003 2004 Vertisol Light soil Low High May June July Ash Animal dung DAP UREA No fertilization Good Intermediate Poor o2800 X2800 Row planting Broadcast Cereals Garlic Onion Potato Brassica Legumes None (fallow) 1 ploughing 2 ploughing 3 ploughing 4 ploughing p30 430
89 100 100 96 188 197 194 191 309 76 6 175 204 25 56 4 52 248 188 79 118 224 161 73 312 22 250 36 11 30 22 14 44 198 137 6 231 154
Year Soil type Crop densitya Planting date
Fertilization
Weed managementb
Altitude (m) Cropping pattern Previous crop
Land preparation
Disease incidence (%) a
Crop density is in m2, lowo33; high X33. Good weeding, any weed is weeded; intermediate weeding, few weeds are present; poor, no weeding and high weed infestation. b
District
Year Soil type Crop densitya Planting date
Fertilization
Weed managementb
Altitude (m) Cropping pattern Previous crop
Land preparation
a
Variable class
Angolela and Asagirt Basona and Werena Lalo Mama Mider Tarmaber 2003 2004 Vertisol Light soil Low High May June July Ash Animal dung DAP UREA No fertilization Good Intermediate Poor o2800 X2800 Row planting Broadcast Cereals Garlic Onion Potato Brassica Legumes None (fallow) 1 ploughing 2 ploughing 3 ploughing 4 ploughing
Disease incidence (%) p30
430
42 39 6 42 120 67 99 88 147 40 1 93 93 10 28 1 27 121 103 27 57 91 96 34 153 118 19 7 13 10 9 11 21 99 66 2
47 61 72 76 77 121 95 103 162 36 5 82 111 15 28 3 25 127 85 52 61 133 65 39 129 132 17 4 17 12 5 11 23 99 70 5
Crop density is in m2, lowo33; high X33.18 plants. Good weeding, any weed is weeded; intermediate weeding, few weeds are present; poor, no weeding and high weed infestation. b
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evaluation of the importance of multiple independent variables that affect the disease incidence. The logit link function was used in this binomially distributed data to determine the effects of the independent variable to the response variable. This type of analysis for determining the association of independent variables with disease incidence and/or severity has also been used by other workers (Twengstrom et al., 1998; Fininsa and Yuen, 2001). The independent variables were evaluated twice for their effect on the incidence of white rot. First, all the independent variables were tested in single variable model (Type 1 analysis). A Type 1 analysis consists of fitting a sequence of models, beginning with a simple model with only an intercept term, and continuing through a model of specified complexity, fitting one additional effect on each step. From this analysis all the parameter estimates were analysed and the likelihood ratio statistics were tested, and the deviance and the Chi-square value were analysed for the significance effect of the independent variables and variable classes on disease incidence. The likelihood ratio statistics was used to examine the importance of variables and was tested against a Chi-square. Those independent variables which showed significant association to the disease incidence were then tested in a reduced model (Type 3 analysis). A Type 3 analysis used likelihood ratios instead of sums of squares. The parameter estimates and their standard error were analysed using the GENMOD procedure both in single and multiple models. The odds ratio was obtained by exponentiating the parameter estimates for comparing the effect based on a reference point. Analysis of deviation was performed for the independent variable in a reduced model. The deviation was used to compare the different models. The analysis and interpretation of the data was done partly based on deriving decision rules (Yuen, 2006). 3. Results 3.1. White rot prevalence and distribution Different levels of white rot incidence were recorded on garlic local cultivars among the districts (Table 5). Mean disease incidence of white rot was 26% at Angolela and Asagirt, 30–53.9% at Basona and Werena, 14–28% at Lalo Mama Mider and 22–42.2% at Tarmaber district. The disease incidences were recorded on mean plant densities of 26.6, 25.3, 26.7 and 27.5 plants m2, respectively. In all fields surveyed in each district, garlic plants were infected with white rot except a few fields in Angolela and Asagirt and Lalo Mama Mider. The incidence in each district was higher in 2004 than in 2003 except Angolela and Asagirt which was about the same in both years (Table 5). The results indicated that 96.6% of the total fields (385) surveyed were infected with white rot. The 3.4% of fields not infected were where garlic had not been planted in the previous year. Mean disease incidence ranged from 21% in Lalo Mama Mider to 42% in Basona and Werena district.
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The disease was significantly higher in Basona and Werena (Tables 4 and 5). In the surveyed districts weather conditions varied among the districts. At Basona and Werena, the temperature ranged from 6 to 19.7 1C during the growing period, which is favourable for sclerotial germination and white rot epidemic development (Fig. 2). The incidence in 2004 was higher by 44–49.5% than in 2003 except in Angolela and Asagirt district (T ¼ 38:94, df ¼ 1, P ¼ 0:000). Disease incidence varied between altitude ranges and it was higher in fields lower than 2800 m.a.s.l. (T ¼ 52:84, df ¼ 1, P ¼ 0:0360). The number of fields falling in each altitude range are presented in Table 4. In the surveyed districts it was observed that three planting months (May, June and July), two types of
Table 4 Number of fields surveyed on garlic fields of white rot (Sclerotium cepivorum) in altitude ranges in four districts of North Shewa highlands, Ethiopia in 2003 and 2004 cropping season District
Year
Angolela and Asagrit Basona and Werena Lalo Mama Mider Tarmaber
2003 2004 2003 2004 2003 2004 2003 2004
Altitude range/ number of fields o2800
X2800
37 38 5 20 26 49 18 7
6 8 44 31 22 3 30 41
Total
Total number of fields
43 46 49 51 48 52 48 48 385
Table 5 Distribution of garlic white rot (Sclerotium cepivorum) in four districts of North Shewa highlands, Ethiopia in 2003 and 2004 cropping season District
Year
Plant density (no./m2)7SE
White rot incidence (%)7SE
Probability value Plant Disease density
incidence Angolela and Asagirt
Basona and Werena
Lalo Mama Mider
Tarmaber
2003
27.4271.16
26.9874.0
2004 Mean 2003
25.6971.04 26.5970.79 28.2171.13
25.0372.98 26.0472.53 30.0373.97
0.72
0.74
2004 Mean 2003
22.3971.13 25.3071.13 27.0171.36
53.9274.18 41.9874.07 14.3374.14
0.00
0.00
2004 Mean 2003 2004 Mean
26.3571.13 26.6770.88 28.6971.14 26.3270.96 27.5170.75
28.3673.00 21.6072.61 22.4572.42 42.2474.26 32.3572.64
0.70
0.00
0.11
0.00
Probability value for plant density and disease incidence (Po0.05, T-test).
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A 25
Max Temp
MIN Temp
400 350
Rainfall (mm)
250
15
200 10
150 100
Temperature (°C)
20 300
5
50 0
0
B 450
25
400 20
300 15
250 200
10 150 100
Temperature (°C)
Rainfall (mm)
350
5
50 0
0
C 25
400 350
Rainfall (mm)
250
15
200 10
150 100
Temperature (°C)
20
300
5
50 0
0
D
25 350 20
Rainfall (mm)
250 15 200 150
10
100
Temperature (°C)
300
5 50 0
0 May
June
July
Aug
2003
Sep
Oct
May
June
July
Aug
Sep
Oct
2004
Fig. 2. Rainfall in (bars) and monthly minimum and maximum temperature (curves) from planting to survey time (May–October) for 2003 and 2004 of survey districts: (A) Basona and Werena; (B) Tarmaber; (C) Angolela and Asagirt; and (D) Lalo Mama Mider.
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planting (row and broadcast), and different type of land preparation system and soil fertilization were practiced (Table 2). The incidence in lower plant density (o33 plants m2) and on garlic plants planted in May was lower and did not exceed 10% (data not shown). In comparison, the incidence reached up to 100% in the June planting in all districts. The incidence of white rot was higher in broadcast (garlic cloves planted without definite rows or spacing) planted fields and with one time ploughing than in row planted and frequently ploughed fields (data not shown). In broadcast planted fields, the incidence was higher by 5% than row planted. Farmers planted garlic as a sole crop and in some fields intercropped with Brassica species. Out of the total fields surveyed, 23 garlic fields were intercropped with Brassica carinta locally known as ‘gomenzer’. In these fields garlic plants were free from white rot incidence. In the area, garlic was planted in rotation with different crops. From the cropping history, it was observed that when garlic was planted in rotation with other crops (non Allium species) the white rot incidence was less compared with garlic continuously grown on the same field. Of the total fields surveyed, 137 fields were continuously planted with garlic. Fields with good weed management practices had lower white rot incidence (Table 7). It appeared that the status of weed infestation had an influence on white rot incidence and a significantly higher incidence (37.7%) was recorded in unweeded fields (T ¼ 33:34, df ¼ 2, P ¼ 0:009). 3.2. Association of white rot with environmental factors and cultural practices The association of all independent variables with white rot incidence is presented in Table 6. The independent variables such as year, district, soil type and weed management were significantly associated with white rot incidence when entered into the logistic regression model as a single variable. However, when all variables entered last into the regression model, only year and weed management remained significant in their association with white rot incidence. Among the independent variables, cropping year was the most important variable in its association with incidence when entered first and last in to the model (w2 ¼ 26:08 and 21.91, 3 df). District and soil type lost their importance when entered into reduced variable model. The independent variables year, district, soil type and weed management were tested in a reduced multiple variable model. The results for analysis of deviation for variable and variable class are presented in Table 7. The deviation analysis of these variables in a reduced multiple variable model showed the importance of their association with incidence. The output from this reduced model indicated the importance of the variables and variable classes. The parameter estimates and standard error and odds ratio are presented in Table 7. The probability of lowest incidence was highly associated with the 2003 cropping season, Angolela and Aasgirt and Lalo Mama Mider district and
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Table 6 Independent variables used in logistic regression model of white rot (Sclerotium cepivorum) and likelihood ratio statistics for twelve variables entered first and last into a model Independent variable
Df White rot incidence LRT Type 1 analysisa
Year 1 District 3 Kebele (farmers association) 23 Altitude 1 Plant density 1 Soil type 1 Previous crop 6 Land preparation 3 Fertilization 4 Planting time 2 Plant spacing 1 Weed management 2
Type 3 analysisb
DC
PR4w2
DC
PR4w2
26.06 9.43 26.05 0.15 1.22 4.17 7.24 1.22 1.48 3.54 1.99 9.49
o0.0001 0.0241 0.2985 0.6997 0.2688 0.0411 0.2993 0.7488 0.8296 0.1701 0.1584 0.0087
21.91 2.97 27.40 0.12 1.08 2.97 9.50 0.91 1.88 4.67 2.65 9.49
o0.0001 0.2269 0.2395 0.7304 0.2987 0.0851 0.1475 0.8234 0.7586 0.0970 0.1036 0.0087
df, degrees of freedom; DC, deviance change; PR, probability of a w2 value exceeding the deviance; LRT, likelihood ratio test. a Type 1 analysis ¼ variable entered first in to the model. b Type 3 analysis ¼ variable entered last in to the model.
good weed management practices. High white rot incidence had high probability of association to Basona and Werena district, vertisol, and poor weed management. The incidence was almost 50% greater in poor weeded fields than better weeded ones. All other variables, cropping patternrow and broadcast, previous crop and ploughing frequency did not show significance association on the incidence of white rot. 4. Discussion The distribution of white rot varied among the districts of North Shewa highlands. In Basona and Werena district the incidence was greater by 10–20.5% than in the other districts. In Basona and Werena district farmers grow garlic as commercial crop in addition to home consumption. Although the disease is a bottleneck to increased production and productivity in the area, the crop has been grown continuously year after year. This continuous growing of garlic leads to accumulation of the white rot sclerotia in the soil that increases occurrence of white rot. Continued growing of Allium species on the same field increases the inoculum level and could result in rapid amplification of the disease in the field (Crowe and Hall, 1980b). The existence of favourable temperatures that ranged from 6 to 19.7 1C during the growing period led to increased sclerotial germination and white rot epidemic development at Basona and Werena. Crowe and Hall (1980a) reported that sclerotial germination occurs between 9 and 24 1C and disease development between 6 and 24 1C. The variation in incidence between districts could also have resulted from differences in soil type and the
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Table 7 Analysis of deviance, natural logarithms of odds ratio and standard error of the selected independent variables in a reduced model analysing white rot (Sclerotium cepivorum) incidence Independent variablea
df
Residual devianceb
White rot incidence LRSc DC
PR4w2
Intercept Year
0 1
532.35 506.26
26.08
o0.0001
District
3
496.84
9.43
0.0241
Soil type
1
494.58
2.26
0.1328
Weed management
2
487.13
7.45
0.0241
Variable class
Estimated
SE
Odds ratioe
2003 2004 Angolela and Asagirt Lalo Mama Mider Tarmaber Basona and Werena Veritysoil Light soil Good Intermediate Poor
0.7255 1.1266 0 0.6367 0.6408 0.8843 0 0.3643 0 0.1627 0.6233 0
0.2957 0.2310 0 0.3018 0.3055 0.3161 0 0.2325 0 0.2484 0.3133 0
2.06 0.32 1 0.53 0.53 0.41 1 1.26 1 0.85 1.86 1
df, degrees of freedom; DC, the changes in deviance; PR, probability of a w2 value exceeding the deviance; SE, standard error of the estimate. Reference group. a Independent variables added in to the reduced model. b Unexplained variations after fitting the model. c Likelihood ratio statistics. d Estimates from the model with the independent variables added in to a reduced model. e Exponentiating the estimates.
garlic cultivars used. The soil in the three districts is a lighter soil compared to Basona and Werena districts. The vertisol favoured the occurrence of white rot. It has been reported that wet soil increased the disease incidence provided that the inoculum levels was sufficient in the soil (Entwistle, 1990). White rot incidence varied between years and altitude ranges. In 2003 the incidence was significantly lower than in 2004. In 2003 the seasonal rainfall was less than 2004 and temperatures were relatively higher. In the 2004 cropping season the weather conditions were more favourable for disease development. On average, the temperature ranged from 7 to 22 1C which was suitable for sclerotial germination and disease development. In the survey districts the elevation increased from 2450 to 3350 m.a.s.l. and most of the field surveyed in Basona and Werena were in the range 2750–2890 m. More disease incidence was observed within this altitude range, indicating that cooler environment may have been favourable for white rot. During the survey it had been observed that higher number of infected plants with white rot symptoms was recorded in densely populated fields than in sparsely populated fields. Although the data was not significant difference, it might be due to secondary infections in the fields. It has also been reported that in a dense population of garlic plants, the incidence increases due to more plantto-plant spread of the S. cepivorum. Uninfected roots within 1 to 2 cm of infected roots in contact with infected roots get colonized by hyphae from infected roots (Scott, 1956; Crowe and Hall, 1980b). Garlic fields intercropped with Brassica crops were almost free from white rot incidence. This might be due
to the biofumigant effect of the Brassica plant due to exudates of glucosinolates from its roots. Glucosinolates might be released from the living plant roots at the time when leaves were removed from the plant by farmers. Brassica species adversely affected the population of pathogens in the soil by releasing biocidal compounds (De Ceuster and Hoitink, 1999; Smolinska, 2000; Coventry et al., 2002; Coventry et al., 2005). White rot incidence was more in unweeded fields where there was competition for soil nutrients, spacing and moisture and as a result, the garlic plants were weak and more prone to the disease due to reduction in plant vigour. S. cepivorum also infects wild plant species (Walker, 1924; Scott, 1956; Coley-Smith, 1959) that may have increased the pathogen inoculum build-up to increase disease incidence in unweeded garlic fields. The survey data analysed using logistic regression analysis indicated environmental and cultural variables that are associated with white rot incidence either singly or in combination. The regression model quantified the relative importance of the variables indicating how much the disease was increased or decreased as a function of the independent variables singly or in combination. However, some variables were confounded by the effect of other variables, which are important to disease development or reduction of the disease. The present study identified that white rot incidence varied among districts, between years and environmental factors, soil type and management practices. The results obtained from this study suggested the importance of research on planting date (in relation to temperature), plant spacing, garlic-Brassica intercropping and other related cultural practices to develop white rot
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management options in the surveyed areas and elsewhere with similar agro-ecological settings. Acknowledgements This research was financed by the Swedish Agency for Research Cooperation with Developing Countries (SIDA/ SAREC) and Haramaya University, Ethiopia. The authors thank Shewanneseh Belay, Bakelo Agricultural Development Station, Bakelo for her assistance in data collection. References Abd-El-Razik, A.A., Shatla, M.N., Rushidi, M., 1973. Studies on the infection of onion plants by Sclerotium cepivorum Berk. Phytopathol 76, 108–116. Andrea, T.B., Emma, Z.M., Carmen, G.C., Ronald, F.C., 1996. The use of arbuscular mycorrhizae to control onion white rot (Sclerotium cepivorum Berk.) under field conditions. Mycorrhizae 6, 253–257. Coley-Smith, J.R., 1959. Studies of the biology of Sclerotium cepivorum Berk. III. Host range, persistence and viability of sclerotia. Ann. Appl. Biol. 47, 511–518. Coley-Smith, J.R., 1987. Alternative methods of controlling white rot disease of Allium. In: Chet, I. (Ed.), Innovative Approaches to Plant Disease Control, vol. 1045. Wiley, New York, USA, pp. 161–177. Coley-Smith, J.R., Holt, J.E., 1966. The production by species of Allium of alkyl sulphides and their effect on germination of sclerotia of Sclerotium cepivorum Berk. Ann. Appl. Biol. 64, 289–301. Coley-Smith, J.R., King, J.E., 1969. The production of species of Allium of alkyl sulphids and their effect on germination of sclerotia of Sclerotium cepivorum Berk. Ann. Appl. Biol. 64, 286–301. Coventry, E., Noble, R., Mead, A., Whipps, J.M., 2002. Control of white rot (Sclerotium cepivorum) with composted onion waste. Soil Biochem. 34, 1037–1045. Coventry, E., Noble, R., Mead, A., Whipps, J.M., 2005. Suppression of Allium white rot (Sclerotum cepivorum) in different soils using vegetable wastes. Eur. J. Plant Pathol. 111, 101–112. Crowe, F.J., Hall, D.H., 1980a. Vertical distribution of sclerotia of Sclerotium cepivorum and host root systems relative to white rot of onion and garlic. Phytopathology 70, 70–73. Crowe, F.J., Hall, D.H., 1980b. Soil temperature and moisture effects on sclerotium germination and infection of onion seedling by Sclerotium cepivorum. Phytopathology 70, 74–78.
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De Ceuster, T.J.J., Hoitink, H.A.J., 1999. Prospects and biocontrol agents as substitutes for methyl bromide in biological control of plant disease. Compost Sci. Util. 7, 6–15. Dennis, A.J., 1986. Botrytis neck rots of onion. Plant disease. /http:// cru.cahe.wsu.edu/CEPublications/eb1359/eb1359.htmlS. Earnshaw, D., McDonald, M.R., Boland, G.J., 2000. Interaction among isolates and mycelial compatibility groups of Sclerotium cepivorum and cultivars of onion (Allium cepa). Can. J. Plant Pathol. 22, 387–391. Entwistle, A.R., 1990. Root diseases. In: Rabinowitch, H.D., Brewster, J.L. (Eds.), Onion and Allied crops. Vol. II: Agronomy. Biotic Interaction, Pathology, and Crop Protection. CRC Press, Boca Raton, USA, pp. 103–154. Fininsa, C., Yuen, J., 2001. Association of maize rust and leaf blight epidemics with cropping systems in Hararghe highlands, eastern Ethiopia. Crop Prot. 20, 669–678. Getachew, T., Asfaw, Z., 2000. Achievements in Shallot and Garlic Research, EARO, Addis Ababa, Ethiopia. Mengistu, H., 1994. Research on vegetables disease in Ethiopia. In: Herath, E., Dessalegne, L. (Eds.), Proceedings of the Second National Horticultural Workshop of Ethiopia, 1–3 December. I AR, Addis Ababa, Ethiopia, pp. 209–215. Mengistu, H., Seid, A., 1993. Outbreak of garlic bulb rots in Ethiopia. Annual Report. Debre Zeit Agricultural Research Centre, Alemaya University of Agriculture, 124 pp. Pinto, C.M.F., Mafia, L.A., Casali, V.W.D., Berger, R.D., Cardoso, A.A., 2000. Production components and yield losses of garlic cultivars planted at different times in a field naturally infested with Sclerotium cepivorum. Int. J. Pest Manage. 46, 67–72. SAS Institute Inc., 2003. SAS/STAT Guide for Personal Computers, version 9.1 edition. SAS Institute Inc., Cary, NC. Scott, M.R., 1956. Studies of the biology of Sclerotium cepivorum Berk. I. growth of mycelium in soil. Ann. Appl. Biol. 44, 576–583. Smolinska, U., 2000. Survival of Sclerotium cepivorum sclerotia and Fusarium oxysporium chlamydospors in soil amended with cruciferous residues. J. Phytopathol. 148, 343–349. Tindall, H.D., 1983. Vegetables in the Tropics. Macmillan Publishing, Hong Kong, p. 28. Twengstrom, E., Sigvald, R., Svensson, C., Yuen, J., 1998. Forecasting Sclerotiina stem rot in spring sown oil seed rape. Crop Prot. 17, 405–411. Walker, J.C., 1924. White rot of Allium in Europe and America. Phytopathology 14, 315–323. Yuen, J., 2006. Deriving Decision Rules. The Plant Health Instructor. DOI:10.1094/phi-A-2006-0517-01.
Crop Protection 26 (2007) 1566–1573 www.elsevier.com/locate/cropro
Association of white rot (Sclerotium cepivorum) of garlic with environmental factors and cultural practices in the North Shewa highlands of Ethiopia Tamire Zewdea,, Chemeda Fininsaa, Parshotum K. Sakhujaa, Seid Ahmedb a
Department of Plant Sciences, Haramaya University, P.O. Box 138, Dire Dawa, Ethiopia b Ethiopian Institute of Agricultural Research, P.O. Box 2003, Addis Ababa, Ethiopia
Received 11 August 2006; received in revised form 15 January 2007; accepted 23 January 2007
Abstract Field surveys were conducted in North Shewa highlands, Amhara state, Ethiopia during 2003 and 2004 main cropping seasons to determine the distribution, prevalence and the association of garlic white rot (Sclerotium cepivorum) incidence with environmental factors and cultural practices. In both years a total of 385 garlic fields were surveyed in four districts, and 96.6% of the fields were infested with white rot. Disease incidence varied among districts and between years, altitude range, soil type and field management practices. The mean disease incidence in 2 years ranged from 21% in Lalo Mama Mider to 42% in Basona and Werena district, where it was significantly higher. The incidence in 2004 cropping season was higher by 37.28% than in 2003. Logistic regression was used to analyse the association of white rot incidence with environmental factors and cultural practices as independent variables. District, cropping year, soil type and weed management practices were significantly associated with white rot incidence in a multiple variable model. Higher incidence of white rot was significantly associated with Basona and Werena district. Lower incidences had a high probability of association with Angolela and Asagirt and Lalo Mama Mider (2003) cropping year and good weed management practices. In a reduced multiple variable model, year and weed management practice were significantly associated with lower white rot incidence. In garlic intercropped with Brassica there was very low disease incidence. The survey revealed high occurrence and distribution of white rot in the study area and effective and feasible management options need to be developed. r 2007 Elsevier Ltd. All rights reserved. Keywords: Abiotic factors; Allium sativum; Garlic; Sclerotium cepivorum; White rot
1. Introduction Garlic (Allium sativum L.) is one of the most important vegetable crops widely grown for use as a flavouring condiment in foods in different parts of the world (Tindall, 1983). Garlic is the second most widely cultivated Allium species in Ethiopia after onion (A. cepa L.). Ambo, Debre Work, Adet, Sinana, and other areas of the Ethiopian highlands produce the bulk of garlic (Getachew and Asfaw, 2000). In North Shewa highlands, garlic and onion are cultivated using rain supplemented by irrigation. However, Corresponding author. Tel.: +251 025 661 07 20; fax: +251 025 661 07 13. E-mail address: [email protected] (T. Zewde).
0261-2194/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2007.01.007
production of garlic is constrained by several biotic and abiotic constraints. Among the biotic constraints, fungal diseases are a major factor affecting production and productivity as well as the quality of garlic in different parts of the country. Among the fungal diseases, rust caused by Puccinia allii and white rot caused by Sclerotium cepivorum Berk. (Coley-Smith, 1987) and neck rot caused by Botrytis allii, B. squamosa and B. cinerea (Dennis, 1986) are the most important ones worldwide including Ethiopia. S. cepivorum produces no functional spores. Instead, it propagates only by the production of circular sclerotia (around 300 mm in diameter) which are produced on roots of decayed host plants (Coley-Smith and King, 1969). The sclerotia germinate and produce mycelium only in response to the presence of Allium root exudates (Coley-Smith and
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Holt, 1966). The germinated mycelia penetrate the root epidermis and invade the cortical parenchyma causing extensive tissue disintegration (Abd-El-Razik et al., 1973). Sclerotia spread in mass through movement of soil, water and in infested plant parts. Once introduced into an area, S. cepivorum is gradually spread by contaminated equipments and planting materials, and slowly the production of garlic in the entire field is threatened. White rot causes important economic losses in garlic production worldwide. In UK, 10% losses (Entwistle, 1990); and in Mexico (Andrea et al., 1996) and Brazil (Pinto et al., 2000) losses up 100% were reported. The disease is also serious in Canada and incidence can exceed 65% in commercial fields (Earnshaw et al., 2000). In Ethiopia, Mengistu and Seid (1993) reported heavy damage to garlic due to white rot. In recent years, white rot has become very important in major production areas of garlic (Mengistu, 1994). The yield loss due it has been found to range between 20.7% and 53.4% (Tamire et al., unpublished data). In Ethiopia, information on the distribution and importance of white rot has not been systematically analysed in major growing areas of the country. As white rot disease has become a recurrent problem in major garlic production areas of the country, information obtained from survey work is important for planning management strategies. Therefore, this study was conducted with objectives to determine the (i) incidence and prevalence of white rot in major growing districts, and (ii) its association with environmental factors and cultural practices.
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Amhara Regional state
Tarmaber
Lalo Mama Mider
Baso & Werena
Angolela & Asagirt
Fig. 1. Map of Ethiopia and the survey districts in the Amhara Regional State.
conducted from 25 September to 15 October in 2003 and 30 September to 20 October in 2004. Over 2 years, a total of 385 garlic fields were surveyed of which 25.9% were in Basona and Werena, 25.9% in Lalo Mama Mider, 24.9% in Tarmaber, and 23.1% in Angolela and Asagirt. In both years white rot was assessed at bulb formation stage (at about 120 d after planting). The areas surveyed and the geographic locations are indicated in Fig. 1.
2. Materials and methods
2.2. Survey methods
2.1. Survey sites
The survey was conducted by inspecting garlic fields, and interviewing growers in the districts. Fields were selected at random from each of the districts at intervals of 5 km along main and feeder roads. In each sample field, three quadrants (1 m 1 m) 5 m apart were sampled by making diagonal moves in the field. The plants in each quadrant were taken as the sample unit. The plant population in each quadrant was counted and the mean plant population density was obtained by averaging the plant population in the three quadrants. Incidence of white rot was assessed by counting the number of plants showing white rot symptoms (such as yellowing, discoloration, bulb rotting, and presence of mycelium and/or sclerotia around the base of the plant) in each quadrant and averages were taken for each field. During the survey, altitude (m), type of soil (vertisol or black soil and light soil), cropping pattern (row or broadcast planting), weed management practices and plant density were recorded for each sampled field. Growers were asked information on cropping system, cultivar, and cultural practices (time of planting, land preparation, previous crop, and disease control practices) employed.
White rot disease surveys in major areas of garlic production in the North Shewa highlands were conducted in four districts (Basona and Werena, Lalo Mama Mider, Tarmaber, and Angolela and Asagirt) of North Shewa highlands in 2003 and 2004 during the main rainy season. The survey districts differed mainly in altitude, weather and soil characteristics (Table 1). The survey was
Table 1 Characteristic features of surveyed garlic fields in four districts of North Shewa highlands, Ethiopia District
Altitude (m)
Annual total rainfall (mm)
Temperature (1C)
Soil type
Angolela and Asagrit Basona and Werena Lalo Mama Mider Tarmaber
600–2750
121–921
5–21.1
Light soil
1545–2960
695–905
6–19.7
Vertisol
1450–2960
725–842
7–17.9
Light soil
1900–3250
800–943
3–15.5
Light soil
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2.3. Data analysis Descriptive analysis was performed on all data collected from each field. In addition, data analysis was conducted to describe the distribution, prevalence and association of white rot incidence in relation to the independent variables listed in Table 2. Where significant difference for disease incidence existed, the mean disease difference were separated using the T-test at Po0:05. In the second analysis, the independent variables and variables class were categorized based on the frequency of fields (Table 2). Disease incidence (the response variable) was classified into a distinct class of bivariate qualitative data using the statistical analysis for science (SAS) procedure (SAS Institute, 2003) of the univariate procedure of disease
incidence as variables. Selected class boundaries were p30% and 430%. Tables of independent and variable classes for disease incidence were constructed to represent the bivariate distribution of the fields. The value corresponding to each independent variable represents the frequency of fields falling in the disease range (Table 3). The association of white rot incidence with the independent variables and variables class were analysed using a logistic regression model with the SAS procedure of the GENMOD procedure (SAS Institute, 2003). The GENMOD procedure estimates the parameters of the model numerically through an iterative fitting process. The GENMOD procedure fits a generalized linear model to the data by maximum likelihood estimation of the parameter. The logistic regression model allows the
Table 2 Categorization of variables used in analysis of distribution of white rot (Sclerotium cepivorum) incidence in four districts of North Shewa highlands, Ethiopia (n ¼ 385)
Table 3 Independent variable by disease contingency table for logistic regression analysis of garlic white rot (Sclerotium cepivorum) during 2003 and 2004 at North Shewa highlands, Ethiopia
Variable
Variable class
Number of fields
Independent variable
District
Angolela and Asagirt Basona and Werena Lalo Mama Mider Tarmaber 2003 2004 Vertisol Light soil Low High May June July Ash Animal dung DAP UREA No fertilization Good Intermediate Poor o2800 X2800 Row planting Broadcast Cereals Garlic Onion Potato Brassica Legumes None (fallow) 1 ploughing 2 ploughing 3 ploughing 4 ploughing p30 430
89 100 100 96 188 197 194 191 309 76 6 175 204 25 56 4 52 248 188 79 118 224 161 73 312 22 250 36 11 30 22 14 44 198 137 6 231 154
Year Soil type Crop densitya Planting date
Fertilization
Weed managementb
Altitude (m) Cropping pattern Previous crop
Land preparation
Disease incidence (%) a
Crop density is in m2, lowo33; high X33. Good weeding, any weed is weeded; intermediate weeding, few weeds are present; poor, no weeding and high weed infestation. b
District
Year Soil type Crop densitya Planting date
Fertilization
Weed managementb
Altitude (m) Cropping pattern Previous crop
Land preparation
a
Variable class
Angolela and Asagirt Basona and Werena Lalo Mama Mider Tarmaber 2003 2004 Vertisol Light soil Low High May June July Ash Animal dung DAP UREA No fertilization Good Intermediate Poor o2800 X2800 Row planting Broadcast Cereals Garlic Onion Potato Brassica Legumes None (fallow) 1 ploughing 2 ploughing 3 ploughing 4 ploughing
Disease incidence (%) p30
430
42 39 6 42 120 67 99 88 147 40 1 93 93 10 28 1 27 121 103 27 57 91 96 34 153 118 19 7 13 10 9 11 21 99 66 2
47 61 72 76 77 121 95 103 162 36 5 82 111 15 28 3 25 127 85 52 61 133 65 39 129 132 17 4 17 12 5 11 23 99 70 5
Crop density is in m2, lowo33; high X33.18 plants. Good weeding, any weed is weeded; intermediate weeding, few weeds are present; poor, no weeding and high weed infestation. b
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evaluation of the importance of multiple independent variables that affect the disease incidence. The logit link function was used in this binomially distributed data to determine the effects of the independent variable to the response variable. This type of analysis for determining the association of independent variables with disease incidence and/or severity has also been used by other workers (Twengstrom et al., 1998; Fininsa and Yuen, 2001). The independent variables were evaluated twice for their effect on the incidence of white rot. First, all the independent variables were tested in single variable model (Type 1 analysis). A Type 1 analysis consists of fitting a sequence of models, beginning with a simple model with only an intercept term, and continuing through a model of specified complexity, fitting one additional effect on each step. From this analysis all the parameter estimates were analysed and the likelihood ratio statistics were tested, and the deviance and the Chi-square value were analysed for the significance effect of the independent variables and variable classes on disease incidence. The likelihood ratio statistics was used to examine the importance of variables and was tested against a Chi-square. Those independent variables which showed significant association to the disease incidence were then tested in a reduced model (Type 3 analysis). A Type 3 analysis used likelihood ratios instead of sums of squares. The parameter estimates and their standard error were analysed using the GENMOD procedure both in single and multiple models. The odds ratio was obtained by exponentiating the parameter estimates for comparing the effect based on a reference point. Analysis of deviation was performed for the independent variable in a reduced model. The deviation was used to compare the different models. The analysis and interpretation of the data was done partly based on deriving decision rules (Yuen, 2006). 3. Results 3.1. White rot prevalence and distribution Different levels of white rot incidence were recorded on garlic local cultivars among the districts (Table 5). Mean disease incidence of white rot was 26% at Angolela and Asagirt, 30–53.9% at Basona and Werena, 14–28% at Lalo Mama Mider and 22–42.2% at Tarmaber district. The disease incidences were recorded on mean plant densities of 26.6, 25.3, 26.7 and 27.5 plants m2, respectively. In all fields surveyed in each district, garlic plants were infected with white rot except a few fields in Angolela and Asagirt and Lalo Mama Mider. The incidence in each district was higher in 2004 than in 2003 except Angolela and Asagirt which was about the same in both years (Table 5). The results indicated that 96.6% of the total fields (385) surveyed were infected with white rot. The 3.4% of fields not infected were where garlic had not been planted in the previous year. Mean disease incidence ranged from 21% in Lalo Mama Mider to 42% in Basona and Werena district.
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The disease was significantly higher in Basona and Werena (Tables 4 and 5). In the surveyed districts weather conditions varied among the districts. At Basona and Werena, the temperature ranged from 6 to 19.7 1C during the growing period, which is favourable for sclerotial germination and white rot epidemic development (Fig. 2). The incidence in 2004 was higher by 44–49.5% than in 2003 except in Angolela and Asagirt district (T ¼ 38:94, df ¼ 1, P ¼ 0:000). Disease incidence varied between altitude ranges and it was higher in fields lower than 2800 m.a.s.l. (T ¼ 52:84, df ¼ 1, P ¼ 0:0360). The number of fields falling in each altitude range are presented in Table 4. In the surveyed districts it was observed that three planting months (May, June and July), two types of
Table 4 Number of fields surveyed on garlic fields of white rot (Sclerotium cepivorum) in altitude ranges in four districts of North Shewa highlands, Ethiopia in 2003 and 2004 cropping season District
Year
Angolela and Asagrit Basona and Werena Lalo Mama Mider Tarmaber
2003 2004 2003 2004 2003 2004 2003 2004
Altitude range/ number of fields o2800
X2800
37 38 5 20 26 49 18 7
6 8 44 31 22 3 30 41
Total
Total number of fields
43 46 49 51 48 52 48 48 385
Table 5 Distribution of garlic white rot (Sclerotium cepivorum) in four districts of North Shewa highlands, Ethiopia in 2003 and 2004 cropping season District
Year
Plant density (no./m2)7SE
White rot incidence (%)7SE
Probability value Plant Disease density
incidence Angolela and Asagirt
Basona and Werena
Lalo Mama Mider
Tarmaber
2003
27.4271.16
26.9874.0
2004 Mean 2003
25.6971.04 26.5970.79 28.2171.13
25.0372.98 26.0472.53 30.0373.97
0.72
0.74
2004 Mean 2003
22.3971.13 25.3071.13 27.0171.36
53.9274.18 41.9874.07 14.3374.14
0.00
0.00
2004 Mean 2003 2004 Mean
26.3571.13 26.6770.88 28.6971.14 26.3270.96 27.5170.75
28.3673.00 21.6072.61 22.4572.42 42.2474.26 32.3572.64
0.70
0.00
0.11
0.00
Probability value for plant density and disease incidence (Po0.05, T-test).
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A 25
Max Temp
MIN Temp
400 350
Rainfall (mm)
250
15
200 10
150 100
Temperature (°C)
20 300
5
50 0
0
B 450
25
400 20
300 15
250 200
10 150 100
Temperature (°C)
Rainfall (mm)
350
5
50 0
0
C 25
400 350
Rainfall (mm)
250
15
200 10
150 100
Temperature (°C)
20
300
5
50 0
0
D
25 350 20
Rainfall (mm)
250 15 200 150
10
100
Temperature (°C)
300
5 50 0
0 May
June
July
Aug
2003
Sep
Oct
May
June
July
Aug
Sep
Oct
2004
Fig. 2. Rainfall in (bars) and monthly minimum and maximum temperature (curves) from planting to survey time (May–October) for 2003 and 2004 of survey districts: (A) Basona and Werena; (B) Tarmaber; (C) Angolela and Asagirt; and (D) Lalo Mama Mider.
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planting (row and broadcast), and different type of land preparation system and soil fertilization were practiced (Table 2). The incidence in lower plant density (o33 plants m2) and on garlic plants planted in May was lower and did not exceed 10% (data not shown). In comparison, the incidence reached up to 100% in the June planting in all districts. The incidence of white rot was higher in broadcast (garlic cloves planted without definite rows or spacing) planted fields and with one time ploughing than in row planted and frequently ploughed fields (data not shown). In broadcast planted fields, the incidence was higher by 5% than row planted. Farmers planted garlic as a sole crop and in some fields intercropped with Brassica species. Out of the total fields surveyed, 23 garlic fields were intercropped with Brassica carinta locally known as ‘gomenzer’. In these fields garlic plants were free from white rot incidence. In the area, garlic was planted in rotation with different crops. From the cropping history, it was observed that when garlic was planted in rotation with other crops (non Allium species) the white rot incidence was less compared with garlic continuously grown on the same field. Of the total fields surveyed, 137 fields were continuously planted with garlic. Fields with good weed management practices had lower white rot incidence (Table 7). It appeared that the status of weed infestation had an influence on white rot incidence and a significantly higher incidence (37.7%) was recorded in unweeded fields (T ¼ 33:34, df ¼ 2, P ¼ 0:009). 3.2. Association of white rot with environmental factors and cultural practices The association of all independent variables with white rot incidence is presented in Table 6. The independent variables such as year, district, soil type and weed management were significantly associated with white rot incidence when entered into the logistic regression model as a single variable. However, when all variables entered last into the regression model, only year and weed management remained significant in their association with white rot incidence. Among the independent variables, cropping year was the most important variable in its association with incidence when entered first and last in to the model (w2 ¼ 26:08 and 21.91, 3 df). District and soil type lost their importance when entered into reduced variable model. The independent variables year, district, soil type and weed management were tested in a reduced multiple variable model. The results for analysis of deviation for variable and variable class are presented in Table 7. The deviation analysis of these variables in a reduced multiple variable model showed the importance of their association with incidence. The output from this reduced model indicated the importance of the variables and variable classes. The parameter estimates and standard error and odds ratio are presented in Table 7. The probability of lowest incidence was highly associated with the 2003 cropping season, Angolela and Aasgirt and Lalo Mama Mider district and
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Table 6 Independent variables used in logistic regression model of white rot (Sclerotium cepivorum) and likelihood ratio statistics for twelve variables entered first and last into a model Independent variable
Df White rot incidence LRT Type 1 analysisa
Year 1 District 3 Kebele (farmers association) 23 Altitude 1 Plant density 1 Soil type 1 Previous crop 6 Land preparation 3 Fertilization 4 Planting time 2 Plant spacing 1 Weed management 2
Type 3 analysisb
DC
PR4w2
DC
PR4w2
26.06 9.43 26.05 0.15 1.22 4.17 7.24 1.22 1.48 3.54 1.99 9.49
o0.0001 0.0241 0.2985 0.6997 0.2688 0.0411 0.2993 0.7488 0.8296 0.1701 0.1584 0.0087
21.91 2.97 27.40 0.12 1.08 2.97 9.50 0.91 1.88 4.67 2.65 9.49
o0.0001 0.2269 0.2395 0.7304 0.2987 0.0851 0.1475 0.8234 0.7586 0.0970 0.1036 0.0087
df, degrees of freedom; DC, deviance change; PR, probability of a w2 value exceeding the deviance; LRT, likelihood ratio test. a Type 1 analysis ¼ variable entered first in to the model. b Type 3 analysis ¼ variable entered last in to the model.
good weed management practices. High white rot incidence had high probability of association to Basona and Werena district, vertisol, and poor weed management. The incidence was almost 50% greater in poor weeded fields than better weeded ones. All other variables, cropping patternrow and broadcast, previous crop and ploughing frequency did not show significance association on the incidence of white rot. 4. Discussion The distribution of white rot varied among the districts of North Shewa highlands. In Basona and Werena district the incidence was greater by 10–20.5% than in the other districts. In Basona and Werena district farmers grow garlic as commercial crop in addition to home consumption. Although the disease is a bottleneck to increased production and productivity in the area, the crop has been grown continuously year after year. This continuous growing of garlic leads to accumulation of the white rot sclerotia in the soil that increases occurrence of white rot. Continued growing of Allium species on the same field increases the inoculum level and could result in rapid amplification of the disease in the field (Crowe and Hall, 1980b). The existence of favourable temperatures that ranged from 6 to 19.7 1C during the growing period led to increased sclerotial germination and white rot epidemic development at Basona and Werena. Crowe and Hall (1980a) reported that sclerotial germination occurs between 9 and 24 1C and disease development between 6 and 24 1C. The variation in incidence between districts could also have resulted from differences in soil type and the
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Table 7 Analysis of deviance, natural logarithms of odds ratio and standard error of the selected independent variables in a reduced model analysing white rot (Sclerotium cepivorum) incidence Independent variablea
df
Residual devianceb
White rot incidence LRSc DC
PR4w2
Intercept Year
0 1
532.35 506.26
26.08
o0.0001
District
3
496.84
9.43
0.0241
Soil type
1
494.58
2.26
0.1328
Weed management
2
487.13
7.45
0.0241
Variable class
Estimated
SE
Odds ratioe
2003 2004 Angolela and Asagirt Lalo Mama Mider Tarmaber Basona and Werena Veritysoil Light soil Good Intermediate Poor
0.7255 1.1266 0 0.6367 0.6408 0.8843 0 0.3643 0 0.1627 0.6233 0
0.2957 0.2310 0 0.3018 0.3055 0.3161 0 0.2325 0 0.2484 0.3133 0
2.06 0.32 1 0.53 0.53 0.41 1 1.26 1 0.85 1.86 1
df, degrees of freedom; DC, the changes in deviance; PR, probability of a w2 value exceeding the deviance; SE, standard error of the estimate. Reference group. a Independent variables added in to the reduced model. b Unexplained variations after fitting the model. c Likelihood ratio statistics. d Estimates from the model with the independent variables added in to a reduced model. e Exponentiating the estimates.
garlic cultivars used. The soil in the three districts is a lighter soil compared to Basona and Werena districts. The vertisol favoured the occurrence of white rot. It has been reported that wet soil increased the disease incidence provided that the inoculum levels was sufficient in the soil (Entwistle, 1990). White rot incidence varied between years and altitude ranges. In 2003 the incidence was significantly lower than in 2004. In 2003 the seasonal rainfall was less than 2004 and temperatures were relatively higher. In the 2004 cropping season the weather conditions were more favourable for disease development. On average, the temperature ranged from 7 to 22 1C which was suitable for sclerotial germination and disease development. In the survey districts the elevation increased from 2450 to 3350 m.a.s.l. and most of the field surveyed in Basona and Werena were in the range 2750–2890 m. More disease incidence was observed within this altitude range, indicating that cooler environment may have been favourable for white rot. During the survey it had been observed that higher number of infected plants with white rot symptoms was recorded in densely populated fields than in sparsely populated fields. Although the data was not significant difference, it might be due to secondary infections in the fields. It has also been reported that in a dense population of garlic plants, the incidence increases due to more plantto-plant spread of the S. cepivorum. Uninfected roots within 1 to 2 cm of infected roots in contact with infected roots get colonized by hyphae from infected roots (Scott, 1956; Crowe and Hall, 1980b). Garlic fields intercropped with Brassica crops were almost free from white rot incidence. This might be due
to the biofumigant effect of the Brassica plant due to exudates of glucosinolates from its roots. Glucosinolates might be released from the living plant roots at the time when leaves were removed from the plant by farmers. Brassica species adversely affected the population of pathogens in the soil by releasing biocidal compounds (De Ceuster and Hoitink, 1999; Smolinska, 2000; Coventry et al., 2002; Coventry et al., 2005). White rot incidence was more in unweeded fields where there was competition for soil nutrients, spacing and moisture and as a result, the garlic plants were weak and more prone to the disease due to reduction in plant vigour. S. cepivorum also infects wild plant species (Walker, 1924; Scott, 1956; Coley-Smith, 1959) that may have increased the pathogen inoculum build-up to increase disease incidence in unweeded garlic fields. The survey data analysed using logistic regression analysis indicated environmental and cultural variables that are associated with white rot incidence either singly or in combination. The regression model quantified the relative importance of the variables indicating how much the disease was increased or decreased as a function of the independent variables singly or in combination. However, some variables were confounded by the effect of other variables, which are important to disease development or reduction of the disease. The present study identified that white rot incidence varied among districts, between years and environmental factors, soil type and management practices. The results obtained from this study suggested the importance of research on planting date (in relation to temperature), plant spacing, garlic-Brassica intercropping and other related cultural practices to develop white rot
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management options in the surveyed areas and elsewhere with similar agro-ecological settings. Acknowledgements This research was financed by the Swedish Agency for Research Cooperation with Developing Countries (SIDA/ SAREC) and Haramaya University, Ethiopia. The authors thank Shewanneseh Belay, Bakelo Agricultural Development Station, Bakelo for her assistance in data collection. References Abd-El-Razik, A.A., Shatla, M.N., Rushidi, M., 1973. Studies on the infection of onion plants by Sclerotium cepivorum Berk. Phytopathol 76, 108–116. Andrea, T.B., Emma, Z.M., Carmen, G.C., Ronald, F.C., 1996. The use of arbuscular mycorrhizae to control onion white rot (Sclerotium cepivorum Berk.) under field conditions. Mycorrhizae 6, 253–257. Coley-Smith, J.R., 1959. Studies of the biology of Sclerotium cepivorum Berk. III. Host range, persistence and viability of sclerotia. Ann. Appl. Biol. 47, 511–518. Coley-Smith, J.R., 1987. Alternative methods of controlling white rot disease of Allium. In: Chet, I. (Ed.), Innovative Approaches to Plant Disease Control, vol. 1045. Wiley, New York, USA, pp. 161–177. Coley-Smith, J.R., Holt, J.E., 1966. The production by species of Allium of alkyl sulphides and their effect on germination of sclerotia of Sclerotium cepivorum Berk. Ann. Appl. Biol. 64, 289–301. Coley-Smith, J.R., King, J.E., 1969. The production of species of Allium of alkyl sulphids and their effect on germination of sclerotia of Sclerotium cepivorum Berk. Ann. Appl. Biol. 64, 286–301. Coventry, E., Noble, R., Mead, A., Whipps, J.M., 2002. Control of white rot (Sclerotium cepivorum) with composted onion waste. Soil Biochem. 34, 1037–1045. Coventry, E., Noble, R., Mead, A., Whipps, J.M., 2005. Suppression of Allium white rot (Sclerotum cepivorum) in different soils using vegetable wastes. Eur. J. Plant Pathol. 111, 101–112. Crowe, F.J., Hall, D.H., 1980a. Vertical distribution of sclerotia of Sclerotium cepivorum and host root systems relative to white rot of onion and garlic. Phytopathology 70, 70–73. Crowe, F.J., Hall, D.H., 1980b. Soil temperature and moisture effects on sclerotium germination and infection of onion seedling by Sclerotium cepivorum. Phytopathology 70, 74–78.
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De Ceuster, T.J.J., Hoitink, H.A.J., 1999. Prospects and biocontrol agents as substitutes for methyl bromide in biological control of plant disease. Compost Sci. Util. 7, 6–15. Dennis, A.J., 1986. Botrytis neck rots of onion. Plant disease. /http:// cru.cahe.wsu.edu/CEPublications/eb1359/eb1359.htmlS. Earnshaw, D., McDonald, M.R., Boland, G.J., 2000. Interaction among isolates and mycelial compatibility groups of Sclerotium cepivorum and cultivars of onion (Allium cepa). Can. J. Plant Pathol. 22, 387–391. Entwistle, A.R., 1990. Root diseases. In: Rabinowitch, H.D., Brewster, J.L. (Eds.), Onion and Allied crops. Vol. II: Agronomy. Biotic Interaction, Pathology, and Crop Protection. CRC Press, Boca Raton, USA, pp. 103–154. Fininsa, C., Yuen, J., 2001. Association of maize rust and leaf blight epidemics with cropping systems in Hararghe highlands, eastern Ethiopia. Crop Prot. 20, 669–678. Getachew, T., Asfaw, Z., 2000. Achievements in Shallot and Garlic Research, EARO, Addis Ababa, Ethiopia. Mengistu, H., 1994. Research on vegetables disease in Ethiopia. In: Herath, E., Dessalegne, L. (Eds.), Proceedings of the Second National Horticultural Workshop of Ethiopia, 1–3 December. I AR, Addis Ababa, Ethiopia, pp. 209–215. Mengistu, H., Seid, A., 1993. Outbreak of garlic bulb rots in Ethiopia. Annual Report. Debre Zeit Agricultural Research Centre, Alemaya University of Agriculture, 124 pp. Pinto, C.M.F., Mafia, L.A., Casali, V.W.D., Berger, R.D., Cardoso, A.A., 2000. Production components and yield losses of garlic cultivars planted at different times in a field naturally infested with Sclerotium cepivorum. Int. J. Pest Manage. 46, 67–72. SAS Institute Inc., 2003. SAS/STAT Guide for Personal Computers, version 9.1 edition. SAS Institute Inc., Cary, NC. Scott, M.R., 1956. Studies of the biology of Sclerotium cepivorum Berk. I. growth of mycelium in soil. Ann. Appl. Biol. 44, 576–583. Smolinska, U., 2000. Survival of Sclerotium cepivorum sclerotia and Fusarium oxysporium chlamydospors in soil amended with cruciferous residues. J. Phytopathol. 148, 343–349. Tindall, H.D., 1983. Vegetables in the Tropics. Macmillan Publishing, Hong Kong, p. 28. Twengstrom, E., Sigvald, R., Svensson, C., Yuen, J., 1998. Forecasting Sclerotiina stem rot in spring sown oil seed rape. Crop Prot. 17, 405–411. Walker, J.C., 1924. White rot of Allium in Europe and America. Phytopathology 14, 315–323. Yuen, J., 2006. Deriving Decision Rules. The Plant Health Instructor. DOI:10.1094/phi-A-2006-0517-01.