http://journals.tubitak.gov.tr/agriculture/ © TÜBİTAK
doi:10.3906/tar-1404-133
Effect of Ditylenchus dipsaci Kühn, 1857 (Tylenchida: Anguinidae) on onion
yield in Karaman Province, Turkey
Elif YAVUZASLANOĞLU1,*, Abdullah DİKİCİ2, İbrahim Halil ELEKCİOĞLU3
1Department of Plant and Animal Production, Technical Sciences Vocational School, Karamanoğlu Mehmetbey University, Karaman, Turkey 2Institute of Science, Karamanoğlu Mehmetbey University, Karaman, Turkey
3Department of Plant Protection, Faculty of Agriculture, Çukurova University, Adana, Turkey
1. Introduction
Turkey is an important dry onion producer and the seventh leading producer after China, India, USA, Iran, Russian Federation, and Egypt with a total production of 1.8 × 106 t in 2012 (TÜİK, 2014). Onions are produced in many provinces of Turkey. Karaman Province, which includes terrestrial and Mediterranean mountain climate properties (Karaman Çevre ve Orman Müdürlüğü, 2007), contributes 12,657 t of dry onions or 0.0131 t/ha (2012 data; TÜİK, 2014). Onions are produced in an approximately 1000-ha area in central villages and in the Ermenek and Ayranci districts of Karaman (2012 data; TÜİK, 2014).
Plant-parasitic nematodes cause 8.8%‒14.6% crop losses annually and total economic yield losses of 100‒157 billion US dollars worldwide (Nicol et al., 2011). Ditylenchus spp., Tylenchus spp., and Paratylenchus spp. were found most frequently and abundantly in the
onion-growing areas of Karaman (Dikici and Yavuzaslanoglu, 2012). The stem and bulb nematode Ditylenchus dipsaci Kühn (Tylenchida: Anguinidae) is the most important nematode pest in a wide range of plants, including onion, garlic, hyacinth, narcissus, and tulip, particularly in temperate regions (Potter and Olthof, 1993; Tenente, 1996). Moreover, the European and Mediterranean Plant Protection Organization (EPPO) has placed D. dipsaci as no. 174 on the A2 list of phytosanitary categorization, which is distributed locally in EPPO countries, and it is regulated as a quarantine pest (EPPO, 1997).
Crop losses differ depending on the initial nematode infection level in host plants. Sturhan and Brzeski (1991) reported crop losses of 60%‒80% in heavily infected fields. Mennan (2001) reported that D. dipsaci caused a 65% yield loss in onion in the Suluova district of Amasya.
Abstract: This study was conducted to investigate the effect of the stem and bulb nematode Ditylenchus dipsaci Kühn (Tylenchida:
Anguinidae) on yield parameters of some onion varieties in Karaman Province, Turkey. Experiments were established in a naturally infested onion field during two consecutive years (2012–2013). Nematode population development was followed at the beginning and end of the experiment. The reproduction rate was also calculated. Onion yield and the representative average diameter and length of the onion cultivar bulbs were determined. Yield parameters of six onion varieties were compared on nematicide-treated and untreated control plots in the experiments. Nematode populations significantly decreased in the nematicide-treated plots at the beginning of the experiment during both growing seasons. The average population density of D. dipsaci was 104 individuals/100 g dry soil in the first year and 68 individuals/100 g dry soil in the second year of the experiment. The initial and final nematode populations were significantly positively correlated with Betapanko, Pan88, and Local variety1 cultivars, whereas they were negatively correlated with the Valenciana cultivar during the first year. This suggests that Betapanko, Pan88, and Local variety1 were susceptible to D. dipsaci, whereas the Valenciana cultivar could have some resistance. The overall reproduction rate of D. dipsaci was negatively correlated with initial population density and was primarily <1, which presumably represented a downward trend in nematode reproduction due to environmental conditions at the end of the experiment in September. Betapanko and Pan88 were susceptible varieties, and stem and bulb nematode caused yield losses of up to 12.93% and 15.33%, respectively; these varieties were considered intolerant. The yield of Local variety1 was positively related with initial nematode population density and it was categorized as tolerant to D. dipsaci.
Key words: Onion, stem and bulb nematode, yield
Received: 28.04.2014 Accepted: 17.11.2014 Published Online: 06.04.2015 Printed: 30.04.2015 Research Article
The aim of the present study was to investigate the effect of D. dipsaci on growth and yield parameters of different onion varieties in a naturally infested field in Karaman Province on the Central Anatolian Plateau of Turkey.
2. Materials and methods 2.1. Experimental site
The experiment was set up in a field naturally infected with D. dipsaci in the Morcalı village of Karaman (37.1108°N, 33.11229°E; 1075.79 m a.s.l.) and in the same plots during 2012 and 2013. Ditylenchus dipsaci was identified based on morphological and morphometric characters (Barraclough and Blackith, 1962).
Monthly mean air temperature, soil temperature at a depth of 20 cm, and total rainfall data are shown in Figure 1 (data from the Turkish State Meteorological Service). Monthly mean temperatures of the air and the soil at a depth of 20 cm changed from ‒1.8 to 25.2 °C and from 2.5 to 27.8 °C, respectively, in 2012–2013. Extremely low temperatures were recorded during November‒March and these increased after March until July, then decreased gradually during the 2 years. Most precipitation was observed in January (45.4 mm), November (44.0 mm), and December (52.8 mm) in 2012, whereas in 2013 most precipitation was observed from the beginning of the year until May (15.2‒71.4 mm).
The soil texture of the field was sand, silt, and clay (20.68%, 34.87%, and 44.44%, respectively), and the field soil was classified as clay soil type. Soil pH was weak
alkaline (7.72), and no salinity problem was detected (electrical conductivity: 146.7 µS/cm). The organic matter content of the soil was low (2.77%). Average CaCO3 and P contents of the field soil were 20.7% and 17.9 mg/kg, respectively.
2.2. Experimental design
The experimental was established in a 32.5 m × 38 m area comprising 84 experimental plots. Each plot area was 11.25 m2 for onion planting, including 10 rows. Rows were each 5 m long with 25 cm between rows and 50 cm between plots. Six commercial onion cultivars, Kantaropu, Betapanko, Valenciana, Pan88, Local variety1 (round-type onion), and Local variety2 (long-type onion), were used in the experiments. The first four cultivars were produced from seed, and the last two were produced from vegetative production material. All cultivars were planted 6 cm apart. Two sets of each cultivar were planted collaterally in nematicide-treated and untreated control blocks with seven replications using a completely randomized block design. Nematicide containing 400 g/L of active fenamiphos was applied to seed pads in the rows at planting at a dosage of 5.04 kg/ha (Roberts and Greathead, 1986; Gray and Soh, 1989; Andres and Lopez-Fando, 1996). The two experiments were set up on 24 and 25 March 2012 and 2013 and harvested on 9 and 21 September 2012 and 2013 during the two onion growing seasons.
2.3. Soil sampling and nematode analysis
The experimental plots were sampled three times each year: after establishment of experimental plots, 1 day
Figure 1. Monthly mean air and 20-cm soil depth temperatures and monthly
total rainfall in Karaman Province during 2012 and 2013 (data from Turkish State Metrological Service). –10 0 10 20 30 40 50 60 70 80
January February March April
May June July
August
September October November December January February
March April May June July August
September October November December
2012 2013
Months Monthly total precipitation (mm) Monthly mean air temperature (°C)
before onion planting (Pi1: initial population 1); 2 weeks later, after planting and nematicide application (Pi2: initial population 2) to see the effect of nematicide on nematode populations; and at the end of the experiment preharvest (Pf: final population). Plants were not available at initial population sampling times, so therefore soil nematode populations were evaluated at all sampling times for comparison.
Soil samples (1 kg) were collected from 15 points representative of the plot from a 20-cm soil depth using a soil corer 2.5 cm in diameter. Nematodes were extracted from 100 g of soil taken from each sample by using the modified Baermann funnel technique (Hooper, 1986). Ditylenchus dipsaci populations were counted in a 50-µL subsample taken from 1 mL of nematode suspension under a light microscope at 20× magnification.
Nematode populations were presented as number of individual nematodes per 100 g of dry soil. Multiplication rates of nematodes were calculated by dividing the nematode numbers/100 g of dry soil in the final population into nematode numbers/100 g of dry soil in the initial population (Pi1/Pi2).
2.4. Plant parameters
Ten onions randomly harvested from each plot were weighed after drying at room temperature in the laboratory. Diameter and length of the 10 sampled onions were recorded (Abd El-Al et al., 2010; Ibrahim, 2010). Yield (t/ha) of each plot was determined, and the increase in yield was calculated considering the yield difference between nematicide-treated and untreated control plots of each replication.
2.5. Statistical analysis
Nematode numbers from Pi1 and Pi2 were compared by applying analysis of variance (ANOVA) and Student’s t-test in nematicide-treated and untreated control plots for both years. Initial and final (Pi1 and Pi2) nematode populations of each cultivar in each year separately and both study years together were compared using multivariate correlation analysis. ANOVA and Student’s t-test were performed to distinguish differences between the yield parameters of cultivars.
Yield (t/ha) and mean diameter and length of onion cultivar data were subjected to multivariate correlation analysis depending on the Pi1 and Pi2 of D. dipsaci for each year separately and both study years together.
3. Results
3.1. Nematode populations
Initial population densities were significantly different after nematicide application (P < 0.05). The first initial population levels (Pi1) of D. dipsaci averaged 87 and 82 individuals/100 g of dry soil in the untreated control
plots and nematicide-treated plots, respectively, for the 2 years. The second initial population levels of D. dipsaci decreased significantly in the nematicide-treated plots (42 individuals/100 g of dry soil), but were detected at high density in the untreated control plots (132 individuals/100 g of dry soil) as an average for the 2 years.
The initial nematode populations (Pi1 and Pi2 together) in both the nematicide-treated and untreated control plots were significantly higher during the first year (104 individuals/100 g of dry soil) than during the second year (68 individuals/100 g of dry soil) (P < 0.05).
A significant, positive polynomial regression was observed between the initial and final nematode populations of the Betapanko, Pan88, and Local variety1 cultivars, whereas a negative polynomial regression was observed for the Valenciana cultivar in the first year (P < 0.05; Figure 2). A significant relationship was determined between Pi1 and Pf for the Valenciana and Local variety1 cultivars and between Pi2 and Pf for the Betapanko and Pan88 cultivars. No relationship was detected in any of the cultivars for the initial and final nematode populations in the second year of the experiment. Only Local variety1 had a significant positive relationship between Pi1 and Pf when data for the 2 years were evaluated together (P < 0.05; R = 0.37).
The initial population (Pi2)/100 g of dry soil and reproduction rate of D. dipsaci in all plots during the 2 years of the experiment were significantly negatively related. The reproduction rate decreased when initial population levels increased (P < 0.05; Figure 3).
3.2. Plant parameters
Yield parameters for the onion cultivars were significantly higher during the second year than during the first year of the experiment. Yield in the first year was 8.3 t/ha, whereas during the second year it was 16.2 t/ha (P < 0.05) for all treatments and cultivars.
The yield parameters for the nematicide-treated and untreated control plots and the yield increase (%) of the onion cultivars are shown in Tables 1 and 2 for both growing seasons. There was no bulb yield difference for the Betapanko cultivar in the first year, and yield in the nematicide-treated plots decreased in Local variety1 and Local variety2 in the second year at rates of 10.52% and 10.50%, respectively. In addition, the yields of other onion cultivars increased in nematicide-treated plots. Bulb yield of the Pan88 cultivar was significantly negatively correlated with the initial D. dipsaci population (Pi1) in untreated plots during the first year. While initial population density increased, onion bulb yield decreased at a rate of 2.08% during the first year (Figure 4). Additionally, a slight negative relationship was detected between bulb diameter (R = 0.57) and bulb length (R = 0.59) in the initial population (Pi1) of D. dipsaci in the Pan88 cultivar.
Similarly, the Betapanko cultivar had a significant negative relationship between initial nematode population and bulb yield for both study years together (Figure 5). No yield loss was recorded in the first year, but a 12.93% yield loss occurred in the second year.
Only the Local variety1 cultivar had a slight significant positive relationship between initial nematode population (Pi1) and bulb yield in the second year. Yield of Local variety1 increased linearly according to the initial population of D. dipsaci (Figure 6).
4. Discussion
The effects of D. dipsaci on the yield of commercial onion cultivars were evaluated using nematicide treatment under Karaman agroecological field conditions.
The nematicide fenamiphos was used effectively to reduce the D. dipsaci populations, and the most effective time for application was at planting (Roberts and Greathead, 1986; Andres and Lopez-Fando, 1996). The significant reduction (48%) in D. dipsaci populations after fenamiphos application in both growing seasons in y = 0 .003 x2 –0.434 x + 8 .668 R² = 0 .620 0 10 20 30 40 50 60 70 80 90 100 0 50 100 150 200 250
Final population (/100 g dry soil)
Initial population (Pi2 ) (/100 g dry soil) c y = –0.000 x2 + 0 .173 x –2.591 R² = 0 .541 0 5 10 15 20 25 30 35 40 45 50 0 100 200 300 400
Final population (/100 g dry soil)
Initial population (Pi1) (/100 g dry soil) d y = –0.000 x2+ 0.297x –1.900 R² = 0 .279 –10 0 10 20 30 40 50 60 70 0 50 100 150 200 250 300
Final population (/100 g dry soil)
Initial population (Pi2) (/100 g dry soil) a y = 0 .001 x2 –0.528 x + 45 .46 R² = 0 .265 0 10 20 30 40 50 60 70 80 90 100 0 50 100 150 200 250
Final population (/100 g dry soil)
Initial population (Pi1) (/100 g dry soil) b
Figure 2. Significant relationship between initial and final populations of Ditylenchus dipsaci on onion cultivars in the 2012 growing
season. a) Betapanko cultivar, b) Valenciana cultivar, c) Pan88 cultivar, d) Local variety1 cultivar.
y = –0.002 x + 0.567 R² = 0.013 0 2 4 6 8 10 12 14 16 18 20 0 100 200 300 400 500 Reproduction rat e
Initial population (Pi2)/100 g dry soil
y = –0.057 x + 8 .817 R² = 0.673 0 2 4 6 8 10 12 0 50 100 150 200
Bulb yield (tone / ha
)
Initial population (Pi1)/100 g dry soil
Figure 3. Relationship between initial population (Pi2) and
reproduction rate of Ditylenchus dipsaci in all plots in the 2 years of the experiment.
Figure 4. Relationship between bulb yield and initial Ditylenchus dipsaci population (Pi1) in the Pan88 cultivar in the 2012 growing
Table 1. Yield parameters of the different onion cultivars in nematicide-treated and untreated control plots in the 2012
growing season.
Onion cultivar Bulb diameter (cm) Bulb length (cm) Bulb yield (t/ha) Yield increase (%)
Tr.* Untr.* Tr. Untr. Tr. Untr.
Kantaropu 3.26 3.54 4.90 4.53 5.2 4.0 30.00 Betapanko 3.11 2.94 4.70 5.12 3.1 3.1 0.00 Valenciana 3.59 3.59 4.69 4.65 7.5 5.3 41.50 Pan88 3.63 3.58 4.50 4.49 04.9 4.8 2.08 Local variety1 4.68 4.55 4.11 4.00 14.1 13.1 7.63 Local variety2 3.20 3.21 7.96 7.58 12.9 12.2 5.73
Tr*, nematicide-treated; Untr*, untreated control plots.
Table 2. Yield parameters of different onion cultivars in nematicide-treated and untreated control plots in the 2013
growing season.
Onion cultivar Bulb diameter Bulb length Bulb yield (ton/ha) Yield increase (%)
Tr.* Untr.* Tr. Untr. Tr. Untr.
Kantaropu 4.83 5.22 6.12 5.91 15.3 14.1 8.51 Betapanko 4.33 4.69 7.26 6.22 13.1 11.6 12.93 Valenciana 4.50 4.92 6.78 6.43 18.6 15.6 19.23 Pan88 5.00 4.13 6.29 7.63 17.3 15.0 15.33 Local variety1 4.83 4.93 6.34 6.71 17.0 19.0 –10.52 Local variety2 4.28 4.50 6.87 6.86 17.9 20.0 –10.50
Tr*, nematicide-treated; Untr*, untreated control plots.
Figure 5. Relationship between bulb yield and initial Ditylenchus dipsaci population (Pi1) in the Betapanko cultivar for both study
years.
Figure 6. Relationship between bulb yield and initial Ditylenchus dipsaci population (Pi1) in the Local variety1 cultivar in the 2013
growing season. y = –0.028 x + 9.576 R² = 0.154 0 5 10 15 20 25 0 100 200 300 400
Bulb yield (t/ha)
Initial population (Pi1)/100 g dry soil
y = 0 .027 x + 16 .69 R² = 0.112 0 5 10 15 20 25 30 35 0 50 100 150 200 250 300
Bulb yield (t/ha)
this study supported the previous observations regarding effectiveness of the nematicide fenamiphos.
Initial nematode population densities in the experiments had a significant relationship with yield reductions. The damage observed could be economically important considering the findings of Seinhorst (1956), who found that 0.2‒1 fourth-stage D. dipsaci larvae/100 g of soil was related to economic damage in onion. Similarly, Palo (1962) reported that 10 D. dipsaci/500 g of soil induced damage and Mennan (2005) recorded damage with 5 D. dipsaci/onion plant.
Significant positive relationships of the initial and final D. dipsaci nematode populations in the Betapanko, Pan88, and Local variety1 cultivars were observed in 2012, which points to susceptibility of the onion cultivars. In contrast, there was a negative relationship in the initial and final D. dipsaci populations in the Valenciana cultivar in the first year. Seinhorst (1967) suggested that the negative relationship between the initial populations and the reproduction rate of D. dipsaci was a complex effect of nematode competition for food and space, hosting ability of the plant, and environmental conditions. The reproduction rates were mostly less than 1, presumably because of the downward movement of the nematodes at the end of the growing season in September, as reported by Dikici and Yavuzaslanoglu (2013).
Cook and Evans (1987) defined tolerance as the ability of a cultivar to maintain yield potential in the presence of nematodes. According to this definition, the Betapanko and Pan88 cultivars were intolerant. Yield in untreated plots decreased depending on the nematode population increase.
The highest yield increase recorded following application of nematicide was in the Valenciana cultivar during both years of the experiment; however, the yield
increase was not related to the initial nematode population in this study.
The Local variety1 yield decrease of 10.52% following nematicide application in the second year was supported by a regression analysis showing a tolerant reaction to D. dipsaci. However, a yield increase was observed during the first year following nematicide application. The higher initial population level during the first year may be responsible for this result; Seinhorst (1965) reported that damage caused by root-feeding nematodes was proportional to their population density.
The Local variety2 and Kantaropu cultivars were not significantly correlated with any of the yield parameters investigated. However, yield increases with nematicide application were comparable with the findings of Tunçdemir (1988), Sturhan and Brzeski (1991), and Mennan (2001).
The study showed that D. dipsaci has a significant effect on yield performance of commercially grown onion cultivars under Karaman agroecological conditions. Preliminary responses of certificated and commercially grown onion cultivars to D. dipsaci were recorded in field conditions in Turkey.
The next phase of the study is to extend the investigation to genetic reactions in other onion cultivars grown commercially in Turkey.
Acknowledgments
The authors thank the Scientific and Technological Research Council of Turkey (TÜBİTAK 3501, Project No.: 111O222) for financial support and Dr. Uğur Gözel (Department of Plant Protection, Faculty of Agriculture, Çanakkale Onsekiz Mart University) for reading the manuscript and for his valuable contributions.
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