In 2002 – 2003, three insecticidal substances were tested for their ability to reduce the damage inflicted on plants of white cabbage by cabbage stink bugs, Eurydema ventrale and E. oleracea (Heteroptera: Pentatomidae). The two cultivars of cabbage tested were: the early cultivar, 'Tucana F1', which requires about 60 days from transplanting to harvest, and the mid-early cultivar 'Hinova F1', which requires about 120 days. In a field experiment, the growth and damage on cabbage plants sprayed with malathion (two sprays), potassium soap [potassium salts of fatty acids] (five sprays), and refined rape oil (five sprays) were compared to the growth and damage on unsprayed plants. Potassium soap and refined rape oil are considered to be environmentally friendly insecticides. In 2002, plants of the cultivar 'Tucana', that were treated with malathion had the highest plant weights [PW], head weights [HW], HW/PW ratio, and the lowest number of frame leaves. In the drier year of 2003, there were no significant differences in damage between the three treatments for either cultivar, except during the last assessment done on 13 August. In 2003, plants of 'Tucana', treated with potassium soap, had the highest PW and HW. The significantly lowest PW and HW values were recorded from the untreated plants. For the cultivar 'Hinova', the PW and HW were heaviest from the plants treated with malathion. In both years, the HW/PW ratio of Hinova (mid-early cultivar) did not differ between treatments, while the plants of 'Tucana' (early cultivar) treated with malathion had the highest ratio. Of the three substances tested, malathion was the most effective at reducing the damage on white cabbage plants caused by cabbage stink bugs. However, in an attempt to reduce the use of synthetic insecticides, instead of malathion, we recommend the use of refined rape oil (49 EUR/ha), as it is as effective as potassium soap (81 EUR/ha), but much cheaper.
Keywords: Eurydema species; insecticidal substances; efficacy; white cabbage; damage
White cabbage (Brassica oleracea L. convar. capitata (L.) Alef. var. alba DC.), an important vegetable in Europe, can be grown under a range of conditions, as it is relatively tolerant of low temperatures. In Europe, white cabbage is grown in the open, and so is exposed to many different pest insects. The insects that cause most problems are diamond-back moth (Plutella xylostella [L.]), cabbage white butterfly (Pieris brassicae [L.]) (Olsson and Jonasson [
Eurydema spp. have been studied intensely in Japan, where two, E. rugosum Motschulsky and E. pulchrum Westwood, are regarded as important pests of cruciferous crops (Ikeda-Kikue and Numata [
The damage currently being inflicted by cabbage stink bugs is attributable both to climate change (Fuhrer [
Our current overall aim is to reduce, or to stop using, highly toxic pesticides. Already, some environmentally friendly methods of pest control are being studied, including the use of parasitoids for the control of cabbage bugs (Kívan and Kiliç [
The aim of this research was to show whether two environmentally friendly insecticidal substances were as effective as the widely used insecticide malathion, in reducing the damage done to cabbage by stink bugs of the genus Eurydema. The two environmentally friendly substances were the potassium salts of fatty acids, known as potassium soap (produced by adding potassium hydroxide to the fatty acids present in animal fats and plant oils), and refined rape oil (Badawy and El-Arnaouty [
The experiment was done during 2002 – 2003 in the experimental field of the Biotechnical Faculty in Ljubljana (46°04′N, 14°31′E), Slovenia, an area with a temperate continental climate.
Three substances with insecticidal properties were tested for reducing stink bug damage on two cultivars of white cabbage. The two cabbage cultivars were the mid-early storage cabbage 'Hinova F
The soil in the experimental field was a heavy clay loam, that had a pH of 7.2, an organic content of 2.5% and had been fertilized in early spring with farmyard manure at the rate of 5 kg/m
In both years, the experimental treatments were allocated at random within each of the three replicated blocks. Each block included four treatments, three substances with insecticidal properties and the untreated control. The four treatments were: (
Table I. Programme of the 'insecticides' applied during 2002 and 2003 to control cabbage stink bugs in the experimental field of the Biotechnical Faculty in Ljubljana, Slovenia. Approximate costs of the insecticide treatments are shown as EUR/ha.
Weeks from transplanting in year Treatment 2002 2003 Potassium soap Rape oil Malathion Control 5 6 Yes Yes Yes No 7 8 Yes Yes No No 9 11 Yes Yes Yes No 11 14 Yes Yes No No 13 16 Yes Yes No No Approximate costs of insecticides used (EUR/ha) 80.5 49.0 42.0 –
To accommodate the two cabbage cultivars, each plot was divided into two subplots. Each sub-plot consisted of three rows of 36 plants, spaced 40 cm apart within the rows and 30 cm apart between the rows. This produced a density of 8.2 plants/m
The percent of damage on the surface of the frame leaves of the plants was assessed 8 times in 2002, and 4 times in 2003. Each assessment was done on one frame leaf, selected at random, from 10 cabbage heads on each sub-plot. As no standard scale exists for rating the damage done by cabbage bugs, we used a slightly modified version of the Stoner and Shelton ([
In both years, all plants of the cultivar 'Tucana' were harvested 9 weeks after transplanting. By this time, most of the cabbage heads had reached maturity. In contrast, plants of the cultivar 'Hinova' were harvested 17 (2002) and 18 (2003) weeks after transplanting. The total weight of the plants [PW] (the weight of head + frame leaves) and the weight of the heads [HW] were recorded from four plants/plot selected at random immediately after harvest. The numbers of frame leaves were counted on the same plants, and then a ratio was calculated between the weight of the heads and the total weight of the plants. This ratio provided a measure of the influence of cabbage bugs in reducing the yield of the cabbage plants. We sought to establish whether the number (or the weight) of the frame leaves increased as the overall amount of damage increased.
Differences in the total weight of the plants, weight of the heads, HW/PW ratio, and feeding damage on the frame leaves of the two cabbage cultivars, each subjected to the four different treatments, were analysed using a general ANOVA (two-way). Prior to analysis, each variable was tested for homogeneity of variance, and those data found to be non-homogeneous were transformed to log(Y) before ANOVA. The values for the HW/PW ratio were transformed to arcsine square root values before analysis. Differences (P < 0.05) between the mean values were identified using Student – Newman – Keuls's multiple range test. All statistical analyses were done using Statgraphics Plus for Windows 4.0 (Statistical Graphics Corp., Manugistics, Inc.). The data are presented as untransformed means ± SE.
In 2002, differences in the mean damage rating were found between treatments (F = 27.10; df = 3,1254; P < 0.0001), dates (F = 37.52; df = 7,1254; P < 0.0001) and cultivars (F = 4.10; df = 1,1254; P = 0.0430), and there was an interaction between treatment and date (F = 3.75; df = 21,1254; P < 0.0001). In 2003, which was a hotter, drier year, differences were recorded only between blocks (F = 11.07; df = 2,475; P < 0.0001) and dates (F = 95.06; df = 3,475; P < 0.0001). In 2002, the cultivar 'Tucana' was damaged less than the cultivar 'Hinova', whereas in 2003 both cultivars had similar levels of damage.
In 2002, the amounts of damage recorded on the cultivar 'Tucana' differed (11 June: F = 3.11; df = 3,99; P = 0.0293, 20 June: F = 2.94; df = 3,99; P = 0.0360, 3 July: F = 3.24; df = 3,99; P = 0.0249, 10 July: F = 2.29; df = 3,99; P = 0.0442) between the treatments on all four assessment dates. The mean damage rating exceeded 2 one only one occasion. At the time of the first assessment, less damage was recorded on the plants sprayed with rape oil than on the untreated plants. At the time of the three other assessments, differences in the levels of damage were recorded only on the cabbage plants that were sprayed with either malathion or rape oil (Figure 1). At the time of the first three assessments, damage on the cultivar 'Hinova' did not differ (11 June: F = 0.59; df = 3,99; P = 0.6219, 20 June: F = 2.57; df = 3,99; P = 0.0580, 3 July: F = 1.39; df = 3,99; P = 0.2508) between treatments (Figure 2). However, in the assessments made between 10 July and 26 August, differences (10 July: F = 6.18; df = 3,99; P = 0.0006, 23 July: F = 7.11; df = 3,99; P = 0.0002; 2 August: P = 0.0007; 13 August: P = 0.0041; 26 August: P = 0.0161) were recorded. The mean damage rating was higher during the fifth to the eighth assessments than during the first four assessments. The mean damage rating exceeded 2.5 only on the plants sprayed with potassium soap. Most damage was recorded on 10 July and 23 July on the plants sprayed with malathion. Potassium soap was most effective against cabbage stink bugs in the assessment made on 2 August. Potassium soap and rape oil were the two most effective substances at the time of the last two assessments. At this time, the damage on the plants treated with malathion was similar to that on the untreated plants.
Graph: Figure 1. Mean damage rating for Eurydema spp. feeding on the frame leaves of the early white cabbage cultivar 'Tucana', subjected to four treatments in 2002. Mean values followed by the same letter do not differ (P ≤ 0.05) according to Student – Newman – Keuls's multiple range test. Bars represent SE of mean damage rating.
Graph: Figure 2. Mean damage rating for Eurydema spp. feeding on the frame leaves of the mid-early white cabbage cultivar 'Hinova', subjected to four treatments in 2002. Mean values followed by the same letter do not differ (P ≤ 0.05) according to Student – Newman – Keuls's multiple range test. Bars represent SE of mean damage rating.
In 2003, there were no differences between treatments at the time of the first (and only) assessment (F = 2,21; df = 3,99; P = 0.0906) made on the cultivar 'Tucana', and during the first three assessments (20 June: F = 0.57; df = 3,99; P = 0.6337, 14 July: F = 0.41; df = 3,99; P = 0.7484, 25 July: F = 1.04; df = 3,99; P = 0.3787) made on the cultivar 'Hinova'. Differences (F = 3.30; df = 3,99; P = 0.0229) were recorded, however, only during the fourth (and last) assessment done on the cultivar 'Hinova', when the cabbage plants sprayed with potassium soap were damaged more than the unsprayed plants (Figure 3). Based on the assessments made on 20 June in both years, the mean damage ratings were lower in 2003 than in 2002. This was not the case on the assessments made on 13 August, however, when the mean damage ratings in all four treatments were similar to those recorded during 2002.
Graph: Figure 3. Mean damage rating for Eurydema spp. feeding on the frame leaves of the two cabbage cultivars, 'Tucana' (T) and 'Hinova' (H), subjected to four treatments during 2003. Mean values followed by the same letter do not differ (P ≤ 0.05) according to Student – Newman – Keuls's multiple range test. Bars represent SE of mean damage rating.
In both years, there were differences between treatments (2002: F = 4.31; df = 3,69; P = 0.0062, 2003: F = 3.07; df = 3,69; P = 0.0303), and cultivars (2002: F = 101.99; df = 1,69; P < 0.0001, 2003: F = 48.22; df = 1,69; P < 0.0001), and an interaction between treatment and cultivar (2002: F = 4.49; df = 3,69; P = 0.0049, 2003: F = 3.90; df = 3,69; P = 0.0107). In 2002, although malathion was the most effective insecticide against cabbage stink bugs on the cultivar 'Tucana', differences were not found between the plants treated with potassium soap and rape oil (F = 9.62; df = 3,33; P < 0.0001) (Table II). For the cultivar 'Hinova', a difference was found only between the plants treated with potassium soap and the untreated plants. The weights of the untreated plants, and the plants treated with either rape oil or malathion, were similar (F = 3.01; df = 3,33; P = 0.0363).
Table II. Mean plant weight (g ± SE) of two cabbage cultivars, 'Tucana' and 'Hinova', subjected to four treatments during 2002 and 2003. Mean values followed by the same letter do not differ (P ≤ 0.05) according to Student – Newman – Keuls's multiple range test.
Cultivar Tucana Hinova Treatment 2002 2003 2002 2003 Control 1010.3 ± 131.3 c 1538.8 ± 100.9 c 3059.2 ± 259.2 a 2509.7 ± 119.7 b Potassium soap 1329.6 ± 149.7 b 2076.8 ± 140.5 a 2250.0 ± 210.1 b 2391.9 ± 215.1 b Rape oil 1285.7 ± 113.3 b 1815.7 ± 65.2 b 2415.8 ± 206.1 b 2553.7 ± 216.3 b Malathion 1888.0 ± 131.2 a 1868.9 ± 89.2 ab 2848.1 ± 176.5 ab 3051.3 ± 98.6 a
In 2003, the heaviest plants of 'Tucana', were harvested from the plots treated with potassium soap and the lightest (F = 5.16; df = 3,33; P = 0.0033) from the untreated plots. Malathion was the most effective insecticide against the cabbage bugs that attacked the cultivar 'Hinova'. The values recorded from the plots sprayed with potassium soap and the rape oil were similar (F = 2.84; df = 3,33; P = 0.0443) to those recorded from the unsprayed plots.
In both years, there were differences in the weights of the cabbage heads between treatments (2002: F = 4.17; df = 3,69; P = 0.0074, 2003: F = 3.56; df = 3,69; P = 0.0164) and cultivars (2002: F = 57.68; df = 1,69; P < 0.0001, 2003: F = 4.54; df = 1,69; P = 0.0351), and an interaction between treatment and cultivar (2002: F = 3.41; df = 3,69; P = 0.0196, 2003: F = 4.05; df = 3,69; P = 0.0087). In 2002, the weights of the cabbage heads in the untreated plots of Hinova, and in the plots treated with either malathion or rape oil, were similar (F = 2.31; df = 3,33; P = 0.0448). The head weights from the untreated plants and from the plants treated with malathion were heavier than those from the plants treated with potassium soap (Table III). In the 'Tucana' sub-plots, the heaviest (F = 9.47; df = 3,33; P < 0.0001) cabbage heads were recorded from the malathion treatment and the lightest from the untreated plants.
Table III. Mean head weight (g ± SE) of two cabbage cultivars, 'Tucana' and 'Hinova', subjected to four treatments during 2002 and 2003. Mean values followed by the same letter do not differ (P ≤ 0.05) according to Student – Newman – Keuls's multiple range test.
Cultivar Tucana Hinova Treatment 2002 2003 2002 2003 Control 692.3 ± 109.7 c 1236.9 ± 91.3 c 2117.6 ± 239.7 a 1810.0 ± 114.5 b Potassium soap 966.1 ± 130.2 b 1732.3 ± 96.1 a 1495.4 ± 154.6 b 1630.8 ± 172.4 b Rape oil 944.9 ± 94.0 b 1551.6 ± 65.9 b 1696.2 ± 202.7 ab 1820.9 ± 213.1 b Malathion 1430.1 ± 109.0 a 1629.6 ± 86.3 ab 2057.2 ± 165.6 a 2401.6 ± 97.7 a
In the Hinova sub-plots in 2003, the cabbage sprayed twice with malathion had the heaviest heads. No differences (F = 4.73; df = 3,33; P = 0.0047) were recorded between the other two treatments and the unsprayed (control) plots. In the 'Tucana' cultivar, the heaviest heads were recorded from the plants treated with potassium soap or malathion, and the lightest from the untreated plants (F = 6.52; df = 3,33; P = 0.0008).
In 2002, different numbers of frame leaves were recorded between blocks (F = 4.66; df = 2,69; P = 0.0111), treatments (F = 6.95; df = 3,69; P = 0.0002), and cultivar (F = 17.01; df = 1,69; P = 0.0001), but only between (F = 6.97; df = 1,69; P = 0.0094) cultivars in 2003. For both cultivars in 2002, most ('Hinova': F = 4.10; df = 3,33; P = 0.0099; 'Tucana': F = 3.33; df = 3,33; P = 0.0247) frame leaves were found on the cabbage plants growing in the unsprayed plots (Table IV). In addition, in the 'Tucana' sub-plots, there were no differences between the plants treated with potassium soap and the untreated plants, whereas the plants treated with malathion had the lowest number of frame leaves. However, in the 'Hinova' subplots, there were no measurable effects from any of the three test treatments. Similarly, during 2003, no differences ('Hinova': F = 1.22; df = 3,33; P = 0.3088; 'Tucana': F = 0.40; df = 3,33; P = 0.7522) were recorded between the treatments applied to either cultivar.
Table IV. Mean number of frame leaves (±SE) on two cabbage cultivars, 'Tucana' and 'Hinova', subjected to four treatments during 2002 and 2003. Mean values followed by the same letter do not differ (P ≤ 0.05) according to Student – Newman – Keuls's multiple range test.
Cultivar Tucana Hinova Treatment 2002 2003 2002 2003 Control 15.4 ± 0.5 a 13.6 ± 0.5 a 14.2 ± 0.5 a 13.6 ± 0.4 a Potassium soap 14.9 ± 0.7 ab 14.0 ± 0.4 a 13.0 ± 0.5 b 13.4 ± 0.6 a Rape oil 14.2 ± 0.4 b 13.9 ± 0.7 a 12.4 ± 0.7 b 12.7 ± 0.3 a Malathion 13.1 ± 0.5 c 14.3 ± 0.5 a 11.9 ± 0.6 b 12.5 ± 0.5 a
In summary, fewest frame leaves were found on the 'Tucana' plants treated with malathion, whereas the numbers of frame leaves on the 'Hinova' plants were similar across all treatments.
Differences in the HW/PW ratio were recorded between blocks (2002: F = 6.12; df = 2,69; P = 0.0028, 2003: F = 3.89; df = 2,69; P = 0.0231) and treatments (2002: F = 2.75; df = 3,69; P = 0.0452, 2003: F = 2.95; df = 3,69; P = 0.0353) in both years. In 2003, there were also differences (F = 40.78; df = 1,69; P < 0.0001) between the cultivars. In the 'Hinova' sub-plots, there were no differences in the HW/PW ratio in either 2002 (F = 0.49; df = 3,33; P = 0.6891) or 2003 (F = 2.32; df = 3,33; P = 0.0836) (Table V). In the 'Tucana' sub-plots, the lowest HW/PW ratio was recorded in both years (2002: F = 5.83; df = 3,33; P = 0.0013, 2003: F = 5.55; df = 3,33; P = 0.0021) from the plants treated with potassium soap. In both years, the plants treated with malathion had the highest ratio. In 2003, the cabbage plants treated with the rape oil also had a high ratio.
Table V. Mean ratio of head weight to total plant weight (±SE) of two cabbage cultivars, 'Tucana' and 'Hinova', subjected to four treatments during 2002 and 2003. Mean values followed by the same letter do not differ (P ≤ 0.05) according to Student – Newman – Keuls's multiple range test.
Cultivars Tucana Hinova Treatment 2002 2003 2002 2003 Control 0.63 ± 0.03 c 0.80 ± 0.02 b 0.66 ± 0.04 a 0.72 ± 0.02 a Potassium soap 0.68 ± 0.03 bc 0.84 ± 0.02 ab 0.66 ± 0.04 a 0.67 ± 0.04 a Rape oil 0.71 ± 0.02 b 0.85 ± 0.01 a 0.67 ± 0.05 a 0.68 ± 0.06 a Malathion 0.75 ± 0.01 a 0.87 ± 0.01 a 0.72 ± 0.03 a 0.78 ± 0.07 a
Although reports of earlier studies indicate several possible ways in which environmentally friendly insecticides could be used for reducing pest insect infestations in cabbage crops, mentions of refined rape oil or potassium soap are rare. Treatment with a mixture of azadirachtin and an organic insecticide, based on potassium soap, killed more diamond-back moth (Plutella xylostella), than either compound alone (Leskovar and Boales [
Our results show that at the time of the early assessments, feeding damage on the frame leaves of white cabbage was similar for all four treatments. Cabbage stink bugs only began to damage plants of the cultivar 'Hinova', during the last 2 weeks of July. Increased damage by cabbage bugs at this time of year was probably related to the nutritional status of the plants during periods of hot weather, and the relative shortage of water at the time of the exponential period of growth of the cabbage plants (Burgess et al. [
In the first three assessments done on the cultivar 'Hinova' we found in both years, that there were no differences between the treatments. We explain this by the fact that at the beginning of the growing period there are few cruciferous crops available and so the numbers of bugs found on cruciferous plants are correspondingly low. This appeared to be particularly true for refined rape oil and potassium soap treatments, which suffocate the insects by blocking their tracheal systems. On the other hand, malathion, an insecticide with contact, stomach and respiratory action, was ineffective against cabbage bug control during the early assessments made in either year. This confirms the findings of earlier studies (Martel et al. [
The heaviest cabbage plants and the heaviest cabbage heads were harvested in 2002 from the plants in the cultivar 'Tucana' that had been sprayed twice with malathion. Plants treated with malathion also had the lowest number of frame leaves, confirming the findings of Poonam, Jasrotia and Suri ([
For the 'Hinova' cultivar, the heaviest plants were recorded surprisingly from the untreated plots. This could have been a result of sensitivity of the cultivars to the test insecticides or to the fact that the plants easily tolerated the levels of damage done by the cabbage bugs in 2002. The highest level of damage was recorded on 2 August and rated at a value of 3.27. We conclude that the high weight of the untreated plants of the cultivar 'Hinova' resulted from the plants having higher numbers of frame leaves, which were also heavier and larger, than those of the cultivar 'Tucana'.
In the summer of 2003, in which the weather was extreme, as there was a severe drought in July and August, differences in plant weight and head weight of the cultivar 'Tucana' were recorded between the plants treated with potassium soap (more effective) and those treated with rape oil. Malathion was most effective when sprayed onto plants of the cultivar 'Hinova'. Previous field studies (Hinks and Spurr [
In the cultivar 'Hinova', the ratio of HW/PW ratio did not differ between the treatments in either year. In the cultivar 'Tucana', all insecticides had a similar influence on the HW/PW ratio. We believe this occurs simply because the growth period of the cultivar 'Tucana' is shorter. Despite the high numbers of frame leaves present on the cultivar 'Tucana', the leaves are small and hence are unable to add sufficient to the overall weight to compensate for the lower weight of the heads.
When the prices of the insecticides are taken into account, it is obvious that two sprays of malathion (42 EUR/ha) is the cheapest treatment, and five sprays of potassium soap (81 EUR/ha) the most expensive. The cost of five sprays of rape oil (49 EUR/ha) is similar to that of the malathion treatment.
We conclude that early cabbage cultivars are less susceptible to cabbage bug infestations, because such plants are colonised only by the relatively few cabbage bugs that manage to overwinter. However, once these bugs start to produce offspring, damage becomes evident on the frame leaves of cultivars, such as 'Hinova', that have a longer growing period. In 2002, when cabbage bugs occurred at a high density, the numbers of frame leaves were highest on the untreated plants. This occurs because cabbage bugs that feed on frame leaves have a greater impact during the early stages of plant growth than during the later stages of growth, when many plants are producing heads. Consequently, when stink bugs damage young plants, there is a decrease in the HW/PW ratio.
Of the insecticides tested, malathion was more effective at reducing infestations of cabbage bugs than the two environmentally friendly insecticides. However, in an attempt to reduce the use of toxic synthetic insecticides, we recommend the use of the two environmentally friendly insecticides and particularly, refined rape oil (49 EUR/ha), as it is considerably cheaper than using potassium soap (81 EUR/ha).
This work was done within Horticulture No P4-0013-0481, a programme funded by the Slovenian Ministry of Higher Education, Science and Technology.
By Stanislav Trdan; Dragan ŽnidarČiČ and Nevenka ValiČ
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