Advances in Applied Agricultural Sciences 2 (2014); 07: 19-36
Effects of some botanical insecticides on wheat insects and their natural enemies in winter and spring wheat
Nabil El-Wakeil 1,2, Nawal Gaafar1,2 and Christa Volkmar 2
1 Pests & Plant Protection Dept. National research Center, Dokki, Cairo, Egypt.
2 Institute of Agric. & Nutritional Sciences, Martin-Luther-University Halle-Wittenberg, Germany.
The efficacy of range of compounds: one botanical insecticide (NeemAzal T/S) and two pyrethroid insecticides, lambda-cyhalothrin (Karate 9.4% S.C) and deltamethrin (Decis2.8% E.C.) were evaluated to control Rhopalosiphum padi (L.) and Metopolophium dirhodum (Wlk.) in laboratory; as well as to control frit fly, Oscinella frit (L.). The later insect was also controlled companying with three species of entomopathogenic nematodes (EPNs) (Steinernema carpocapsae, S. feltiae and Heterorhabditis bacteriophora). Management of wheat midges with different botanicals was also studied; Karate(pyrethroid), Biscaya (neonicotinoid) and NeemAzal T/S (botanical insecticide) which were sprayed on wheat at heading stage (GS 55). Different concentrations were used to study efficiency of the tested compounds on both aphid species 24, 48 and 72 hours post treatment in the laboratory. While frit fly and wheat midges were managed in winter and spring wheat fields and evaluated after 3, 7 and 15 days after botanicals application. Surveying wheat insects and the associated natural enemies were inspected before and after treating of botanical insecticides. The mortality reached 100% after 24 h in M. dirhodum and after 48 h in R. padi. Most of the tested compounds caused acceptable levels of cereal aphid’s control. All treatments induced reduction in frit fly infestation and increased larval mortality as well. Populations of frit-fly larvae were lower in the treated than untreated plots. H. bacteriophora was more efficacious against O. frit in laboratory than S. carpocapsae, while the latter was more efficient in field experiments. Karate resulted in significantly lower population densities of frit fly. Insecticide applications to fields of midge-infested winter wheat significantly reduced the wheat midge damage. There were significant differences in wheat midge numbers between treated and untreated. Lacewings and dance flies were more susceptible; while spider, syrphids and parasitoid wasps were more tolerant. The results indicated that the tested compounds were effective against frit fly, aphids, thrips, leafhoppers and wheat midges; and may be used as alternative control methods in IPM programs. Compatibility between natural insecticides and natural enemies is highly required to keep the environment clean.
Wheat (Triticum spp.) is a cereal crop cultivated worldwide. Wheat insect pests and their natural enemies are evident in many wheat fields in central Germany. Pests can cause great damage during the heading and flowering phases of wheat (Freier et al.2007). Wheat productivity is seriously affected by different wheat insects.
Oscinella frit is an economic pest to wheat, barley, oats, rye and other cereal grains in many places over the world (El-Wakeil et al.2009). Frit fly overwinters as a larva within the stems of cereals (Lindblad 1999) and pupates in spring. Adults emerge in early summer and migrate by flight from overwintering sites to spring cereals where the females oviposit (Tolley and Niemzcyk 1988). Damaged plants produce small panicles which mature late causing high yield losses (Lindblad and Sigvald 1999). Because insecticides are known to cause many problems, many studies are looking for controlling Dipterans with alternative friendly methods (i.e. biocontrol); specifically entomopathogenic nematodes (EPNs), which serve as alternatives, for chemical insecticides (Toledo et al. 2005; Hussein et al. 2006).
Wheat aphids are considered one of most destructive insects in wheat (Dewar and Carter 1984; Steffey and Gray 2012). R. padi, M. dirhodum, and Sitobion avenae have been studied extensively to determine possible yield losses following crop infestations (Dixon 1987; Poehling et al.2007). Forecasting systems based on threshold damage have also been developed to assess possible yield losses (French et al. 2001; Freier et al.2007).
Thrips cause evident damage to winter wheat, whose development most closely overlaps with the life cycle of thrips. The common thrips species are Limothrips denticornis (Hal.), L. cerealium (Hal.) and H. aculeatus (Fab.)(Parrella and Lewis 1997; Mound 2005; Moritz 2006). Both adults and larvae impact winter wheat development, the latter being more destructive by affecting partial or complete white ear effect, drying of flag leaf, partial ear fertilization, and incomplete grain filling (Volkmar et al. 2009;Gaafar 2010).
Among the insect biocenoses that damage winter or spring wheat agroecosystems, leafhoppers have a very important place. Leafhoppers include about 160 genera comprising almost 2000 phytophagous leafhopper species distributed world-wide (Holzinger et al. 2002; Ceotto and Bourgoin 2008). The majority of leafhoppers (Javesella pellucida, Macrosteles laevis, Psammotettix alienus) found on cereals; the later is considered a biological vector for pathogen agents, particularly for viruses (Manurung 2002; Bressan et al. 2009; Finger et al.2012). Cereal leaf beetles, Oulema melanopus (L.), feed in the spring on developing winter wheat. In the fall, adults feed but do not reproduce on corn leaves (Frank et al. 2012).
Orange wheat blossom midge (WBM), Sitodiplosis mosellana (Géhin), and yellow wheat blossom midge, Contarinia tritici (Kirby) (Diptera: Cecidomyiidae), are among the major pests of wheat ears of spring and winter wheat (Oakley et al. 1998; Volkmar et al. 2008; Gaafar et al. 2011). Attack by wheat blossom midges decreases grain germination capacity (5-10%), grain and flour yield and decreases the quality of the harvested grain (Lamb et al. 2002). Effective application of insecticides is possible by using monitoring traps daily of adults and subsequent adjustment of pesticide sprayings. However, insecticides destroy natural enemies (Elliott 1988; Ellis et al. 2009).
Risk assessment procedures for determining pesticide effects on wheat insect natural enemies involve three tiers of testing: at the laboratory, semiﬁeld and ﬁeld levels (Croft and Whalon 1982; Smith and Straton 1986; Holland et al. 2000). A database of insecticide toxicity to non-target invertebrates (insects and spiders) was compiled (Theiling and Croft 1988; Longley and Jepson 1996; El-Wakeil et al. 2013a). For field applications another important factor influencing the outcome is the size of the treated area and the potential for reinvasion by individuals from untreated areas (Carter 1987;Sigsgaard 2002; Schmidt et al. 2004; Steffey and Gray 2012).
We hypothesize that, following botanical insecticides application alone or combination with entomopathogenic nematodes on winter or spring wheat, both wheat insect pests and natural enemy populations will be partially depleted in the treated plots. This study aimed to study insecticide impacts on wheat insect pests and their associated natural enemies in winter and spring wheat.
Materials and Methods
Wheat plants and cereal aphids: Wheat, Triticum aestivum was sown in small pots in the controlled greenhouse. The wheat plants (3-week old) were used in bioassay studies. Susceptible strains of R. padi and M. dirhodum were populated on wheat plants till having sufficient aphids to start the experiments. Young apterous females (4th instar) were used.
Tested compounds: Two botanical insecticides are NeemAzal T/S (10.6 g/l Azadirachtin) (50, 100, 200, 300, 400 and 500 µl) which was provided by Trifolio–M GmbH, Germany. The two pyrethroid insecticides are Karate (9.4 % S.C lambda-cyhalothrin) (0.3, 0.6, 1.25, 2.5, 5 and 10 ppm) and Decis (deltamethrin 2.8 % E.C.) (2.5, 5, 10, 20, 30 and 40 ppm).
Bioassay studies of tested compounds: Wheat leaves were dipped in the prepared insecticidal solution for 10 seconds then left to dry. Then leaves were placed upside down in a small Petri dish (10 mm diameter); ten healthy apterous adults were placed on the treated leaves surface. Leaves dipped in tap water were used as control. Three replicate batches of aphids (i.e. 30 insects) were used per each concentration. Petri dishes containing aphids were carefully closed and kept to count mortality percents (24, 48 and 72 hours after application). The mortality percents were corrected according to Abbott’s formula (Abbott 1925).
Frit fly, O. frit
Nematodes: EPNs for field trials (Steinernema feltiae, S. carpocapsae and Heterorhabditis bacteriophora) were obtained from company e-nema GmbH, Germany that had been cultured in liquid media according to the method described by Ehlers (2001).
Karate: 9.4 % S.C Lambda-cyhalothrin
Treatments: The EPNs and λ-cyhalothrin were sprayed in the field on 23rd April & 7th May 2009, and 29th April & 13th May 2010 at growth stages 11 & 20, respectively. Nematode suspensions of S. feltiae, S. carpocapsae and H. bacteriophora were sprayed with application dose 2.5 x 109 IJs/ ha, and applied to wheat plants naturally infested with O. frit. The control plots were sprayed with water.
Spring wheat plots: The experiments were conducted in Julius Kühn field (sandy loam soil) in Halle, Germany. An Egyptian wheat variety (Sakha 93), in addition to a German variety (Triso); both were cultivated at end of March in 2009 and 2010. The experimental area was a randomized complete block design with 4 blocks and plot size is 3×8 m. In each block, variables (5 treatments and 2 wheat varieties) were distributed randomly; each treatment was replicated 4 times.
Frit flyinfestation: Inspection of infestation was carried out just before spraying and 3, 7, 10, 15 days after both sprays by investigating 10 plants randomly from each plot (total 40 plants/ treatment). All sampled plants were examined visually for infestation symptom (yellow or missing central leaf).
Frit fly larval mortality: Frit fly larvae were counted by dissecting 10 infested tillers in each plot (40 plants/ treatment). These larvae were observed whether they were alive or dead to calculate the mortality % after 3 & 10 days of both sprays. Dead larvae were dissected once again in nematode treatments after 7days to confirm that the death was due to EPNs.
Wheat blossom midges
Winter wheat field: The experiments were conducted during the 2012 summer vegetation period in Bad Lausick, Germany. The wheat variety “Kerubino” was chosen for these experiments (Anonymous 2011). The experimental plot is 16m (long) by 24m (wide); these plots were placed in a randomized completed block design (four blocks), each treatment was repeated three replicates in each block.
Chemical control: The wheat midge management was conducted by using Karate (9.4 % S.C Lambda cyhalothrin), a pyrethroid insecticide, at a rate of 0.75l/ ha (Anonymous 2012), and Biscaya a neonicotinoid insecticide (240g/L thiacloprid) at rate of 0.4 L/haand NeemAzal T/S a botanical insecticide (10.6 g/l Azadirachtin) at rate of 3L/ 500L water/ ha. The tested compounds were sprayed on 6th June 2012 at heading stage (GS 55). Midges were sampled before the insecticide application, thereafter, 7, 15, 21 and 28days after treatment. The mortality or reduction percents were calculated based on Abbott (1925).
Surveying wheat midge larvae using water traps
White water traps: The migrated orange and yellow midge larvae from wheat ear were monitored during their wander to soil. The traps consisted of white plastic dishes; 12.5cm diameter and 6.5cm deep. In each plot, three traps were placed and partly filled with water plus drops of detergent at GS 71 till 85. The traps were observed weekly; and the caught larvae were counted using a binuclear in the lab (Barker et al. 1997).
Yellow water traps: Three yellow water traps/ plot were placed between plants. The trapping fluid consisted of water with a drop of detergent. This method is designed to identify larvae of orange and yellow wheat midges. The collected samples were transferred in 100 ml plastic cups with ethanol; these traps were gathered weekly and identified in the lab.
Inspecting wheat midge adults using sticky traps: Sticky traps (Pherocon AM No Bait traps, Trece Inc., CA, USA (dimensions of the sticky trap is 21 x 27cm) are fastened onto bamboo stakes. Three traps are placed at the same height as the wheat heads in each plot (Lamb et al. 2002). Weekly, traps were collected, and adult of wheat midges on each trap was counted.
Wheat insect pests and the associated natural enemies
Wheat plots and chemical used: Wheat plots (see 2.3.1); Karate,Biscayaand NeemAzal T/S were sprayedat rate of (75ml/ ha, 0.4 L/ha and 3L/ ha, respectively) on 8th May at growth stage 32 and on 6th June at heading stage (GS 55); Biscaya was only sprayed at the heading stage.
Population of wheat insect pests and natural enemies: Insect populations (aphids species, thrips species, leafhopper species, cereal leaf beetle and cereal bugs) and their associated natural enemies (such as predators (lady beetles, lacewings, syrphids, dance flies and spiders), and parasitoids (parasitic wasps)) were sampled and counted using sweep net method (number of sweeps per sample: two 25-sweeps (35cm diameter) before and after insecticide applications (3, 7, 10, 15, 21 and 28 days). The contents were then examined and species and genera identified based on method of Schmidt et al. (2004). The mortality or reduction percents were calculated based on Abbott (1925).
Statistical analysis: The effect of treatments on individual wheat insect populations and parasitoids and predators were analysed using Statistix 9 and performed with the General Linear Model procedure with treatment as the fixed effect and attention to different observation dates (Thomas and Maurice 2008). Percentage data were arcsine transformed prior to analyses. The Factorial Design procedure computes the analysis of variance for complete factorial designs and interprets factorial experiments in a randomized block design with replication. A large F test and corresponding small p-value (P < 0.05) is evidence that there are differences, and using Tukey test to compare means of treatments and inspection dates.
Cereal aphids (Bioassay of tested compounds on the cereal aphids)
Karate treatment: Mortality of R. padi ranged from 19.3 to 86.7% at rate of 0.3 and 10 ppm post 24 hrs, while ranged from 33.3 to 100% after 48 hrs and from 41.6 to 100% post 72 hrs at rate of 0.3 and 10 ppm, respectively. Mortality of M. dirhodum ranged from 26.7 to 100 % at rate of 0.3 and 10 ppm post 24 hrs, while ranged from 39.2 to 100 % after 48 hrs and from 62.5 to 100% post 72 hrs at rates of 0.3 and 10 ppm, respectively (Table 1).
Decis treatment: Mortality of R. padi ranged from 13.9 to 82.7 % at rate of 5 and 40 ppm post 24 hrs, while ranged from 18.6 to 96.3 % after 48 hrs and from 40 to 100 % post 72 hrs at rate of 5 and 40 ppm, respectively. Mortality of M. dirhodum ranged from 14.8 to 85.2 % at rate of 2.5 and 30 ppm post 24 hrs, while ranged from 43.9 to 100 % after 48 hrs and from 62.5 to 100 % post 72 hrs at rate of 2.5 and 30 ppm, respectively (Table 1).
NeemAzal T/S treatment: Mortality of R. padi ranged from 0.0 to 46.4% at rate of 50 and 500µl post 24 hrs, while ranged from 6.7 to 65.4 % after 48 hrs and from 16.7 to 87.8 % post 72 hrs at rate of 50 and 500 µl, respectively. Mortality of M. dirhodum ranged from 0.0 to 40.8 % at rates of 50 and 400 µl post 24 hrs, while ranged from 11.5 to 73.1 % after 48 hrs and from 20.9 to 95.9 % post 72 hrs at rates of 50 and 400 µl, respectively (Table 1).
Generally, M. dirhodum was more susceptible than R. padi. The mortality reached to 100 % after 24 h on M. dirhodum, while achieved on R. padi after 48 h. The highest mortality was recorded in pyrethroids (Karate, then Decis) compared to NeemAzal T/S. The best concentrations were in Karate (10 ppm), Decis (30-40 ppm) and NeemAzal T/S (400-500 µl) (Table 1).
Effects of companying EPNs and Karate for controlling frit fly
Frit fly infestation percents in the field experiments
A. 2009: After the first spray, the percent infestation significantly differed between treatments (P=0.001); they were higher in control than the treated plots. There was a significant difference (P= 0.002) between λ-cyhalothrin and EPNs treatments (these percents were lower in λ-cyhalothrin than EPNs plots). Among EPNs nematodes, there was a significant differences (P=0.0131), where the lowest infestations were recorded in S. carpocapsae plots compared to S. feltiae and H. bacteriophora, especially in Sakha 93 variety (Fig. 1A). Data analyses showed that there were significant differences between wheat varieties (P= 0.002); the infestation percents in Sakha 93 variety were higher than Triso variety (Fig. 1A).
Fig. 1.Effects of entomopathogenic nematodes and Karate on O. frit percent infestation before and after 3, 7, 10 and 15 days: (A) 1st spray on 23 April and (B) 2nd spray on 7 May 2009 in 2 wheat varieties. Different letters indicate significant differences.
After the second spray, percent infestation significantly differed (P=0.001) between treatments; where λ-cyhalothrin and S. carpocapsae were more efficient in reducing the percent infestation than S. feltiae and H. bacteriophora. The percent infestation of O. frit reduced regularly with days post treatment (Fig. 1B). The analyses of data showed that there were significant differences between wheat varieties (P=0.003); the Sakha 93 variety had received infestation percents higher than Triso variety (Fig. 1B).
B. 2010: There were significant differences in percent infestation (P=0.002) between treatments; where λ-cyhalothrin had the lowest percent infestation, followed by S. feltiae and S. carpocapsae which had the greatest infestation than H. bacteriophora after the first spray. The percent infestation significantly differed (P=0.0016) between varieties; Sakha 93 had infested tillers more than Triso (Fig. 2A).
Fig. 2.Effects of entomopathogenic nematodes and Karateon O. frit percent infestation before and after treatments in two wheat varieties: (A) 1st spray on 29 April and (B) 2ndspray on 13 May 2010. Different letters indicate significant differences.
After the second spray, there was a significant difference (P=0.014) between λ-cyhalothrin and EPNs treatments (these percents were lower in λ-cyhalothrin than EPNs plots). Among EPNs nematodes, there was a significant difference (P=0.0025), where the highest infestations were recorded in H. bacteriophora plots compared to S. carpocapsae and S. feltiae; the later 2 species have the same percent infestation in the 2010 (Fig. 2B). The percent infestation significantly differed between varieties (P= 0.0192); they were lower in Triso than in Sakha 93 variety (Fig. 2B).
Frit fly larval mortality percents in the field experiments
A. 2009: After the first spray, the larval percent mortality was significantly different (P= 0.0001) among EPNs treatments after 3 & 10 days, where percent mortality after 10 days were higher than after 3 days. There was no significant difference (P=0.061) between two dates in λ-cyhalothrin plots. In Sakha 93 variety, S. carpocapsae achieved greater larval percent mortality 60% after 10 days than other treatments, while λ-cyhalothrin caused 53.3% on 10th day (Fig. 3A). In Triso variety, λ-cyhalothrin accomplished the highest larval percent mortality 53.3% on both dates, followed by S. carpocapsae which had caused mortality (37 and 43.3%) after 3& 10 days, respectively (Fig. 3A).
Fig. 3. Mean ± SE of O. frit larval percent mortality in infested tillers in two spring wheat varieties after entomopathogenic nematodes and Karate treatments: (A) 1st spray on 23 April and (B) 2nd spray on 7 May 2009. Different letters indicate significant differences.
After the second spray, there were significant differences between percent mortality after 3 & 10 days (P=0.001) in EPNs plots, where mortality after 10 days was greater than after 3 days. The larval mortality did not differ significantly (P=0.0757) between two dates in λ-cyhalothrin plots. The highest larval mortality was recorded in S. carpocapsae plots; 70% after 10 days than other treatments, while λ-cyhalothrin had caused 68% mortality after 10 days, respectively in Sakha 93 variety (Fig. 3B). While in Triso variety, the greatest percent mortality was recorded in λ-cyhalothrin (63 and 68%) after 3 and 10 days, followed by S. carpocapsae which caused 57 and 63.3% mortality after 3 & 10 days, respectively (Fig. 3B).
mortality after 3 & 10 days, respectively (Fig. 3B). larval percent mortality (P=0.001) among treatments after the 1st spray; the highest mortality was found in treated compared to control plots. Among EPNs treatments, percent mortality was significantly higher (P=0.002) in S. feltiae and S. carpocapsae than H. bacteriophora. There were significant differences (P=0.0011) in larval mortality between the investigation dates (3rd and 10th); the highest mortality was recorded on the 10th day compared to 3rd day (Fig. 4A).
Fig. 4.Mean ± SE of larval percent mortality in infested wheat tillers in two spring wheat varieties after entomopathogenic nematodes and Karate treatments: (A) 1st spray on 29 April and (B) 2nd spray on 13 May 2010. Different letters indicate significant differences
After the 2nd spray, the larval percent mortality was significantly different (P=0.001) between treated and control plots; λ-cyhalothrin had the highest mortality percents, followed by both Steinernema species compared to the others (Fig. 4B). There were significant differences between percent mortality (P=0.001) among EPNs treatments after 3 and 10 days; where mortality after 10 days was higher than after 3 days. The highest larval mortality was recorded in S. carpocapsae and S. feltiae plots than H. bacteriophora (Fig. 4B).
Effects of botanical insecticides on orange and yellow wheat midge larvae
White water traps
Both orange and yellow wheat midge larvae were surveyed by white water traps during their way immigrating to the soil at end of wheat season. Generally, the results showed that midge larvae in control plots were significantly different (P= 0.001) than treatments, within the different treatments were Karate and Biscaya had a good influence on wheat midge populations than NeemAzal T/S treatments (Fig. 5A).
Fig. 5. Mean population ± SE of orange & yellow wheat midge cached by (A) white water Traps, (B) yellow water traps and (C) sticky traps (n= 12) after insecticides application. Different letters indicate significant differences.
In general, the results proved that larvae of idges in treatments plots were significantly lower (P= 0.0011) than control plots. Within the treatments, Karate caused the highest percent mortality of wheat midges than other both treatments (Fig. 5B).
Effect of insecticide application on wheat midges using sticky traps
Both adults of orange and yellow wheat midges were surveyed by sticky traps. Generally, the results showed that midge adults in control plots differed significantly (P= 0.0022) than treatments, within the different treatments, midge adults were higher in NeemAzal T/S than Karate and Biscaya (Fig. 5C).
Effect of insecticides on wheat midge larvae and adults (Mortality %- Abbott value)
There were considerable significant differences in the impact of insecticide on wheat midge larvae and adults as shown in Table (2). In white water trap results, Karate caused the highest percent larval mortality (72.8%), followed by Biscaya (57.2%) then came NeemAzal T/S (46.8%). While in yellow water traps, the larval mortality percents differed significantly (P= 0.001); they were recorded as the followings: 66.7, 54.5 and 45.5 % in Karate, NeemAzal T/S and Biscaya, respectively. The reduction percents in wheat midge adults were significantly different (P= 0.002), these percents reached to 45.4% in NeemAzal T/S, 57.4% in Biscaya and 66 % in Karate as found by using sticky traps.
Table 2:Effect of botanical and synthetic insecticides on wheat midges (Abbott values in %) population surveyed by white and yellow water traps as well sticky traps
Karate caused the highest percent reduction of aphids, with a 73.4% reduction after the first spray period and 66.4% after the second spray period. In NeemAzal T/S-treated plots, percent reduction was 22.1% after the first sample period and 23.3% after the second sample period. There were significant differences in percent mortality of thrips between control and treatments (P= 0.0013). Cereal leaf beetle mortality significantly differed between treatments (P= 0.01) and percent reduction was higher in Karate plots compared to NeemAzal T/S plots. Percent mortality in leafhopper was 52.3 after the first spraying period and 31.7% after the second spraying period in Karate plots, while percent reduction in NeemAzal T/S was 30.2% after the first spraying period and 3.8% after the second spraying period. Percent mortality of cereal bugs was higher in Karate than in NeemAzal T/S plots. Click beetles also affected by insecticidal treatments (Table 3).
B. After two sprays: The same trend mentioned above was also recorded after two sprays; Karate achieved the highest percent mortality for aphids, thrips, cereal leaf beetle, leafhoppers and bugs, except click beetles whereas Biscaya caused the highest percent. NeemAzal and Biscaya caused the same mortality level for thrips, cereal leaf beetle, leafhoppers and bugs; except aphids while it was higher in Biscaya than NeemAzal (Table 3).
Effects on natural enemies
A. After one spray: The highest percent mortality was found by Karate for coccinellids and dance flies (66.7 and 64.0%) after the first sample period. The lowest percents were recorded by NeemAzal for lacewings and syrphids (3.5 and 7.1%) after the second sample period (Table 4).
B. After two sprays: Percent mortality by Karate was recorded as the following: 60.9, 54.5, 59.2, 55.8 and 60.6 percent for coccinellids (adults+ larvae), dance flies, syrphids, lacewings and staphylinids, respectively; while these percent were lower for spider and parasitoid wasps (35.5 and 32.2%). NeemAzal T/S and Biscaya caused almost the same side effect on most of these natural enemies (Table 4).
Effects on the cereal aphids
R. padi and M. dirhodum caused significant damage (in statistical and economic terms) on wheat plants under greenhouse conditions. It is noted that the both of cereal aphids show quite different reactions to tested compounds. One possible explanation for the lesser impact of the concentrations on R. padi than M. dirhodum is due to different behaviour of both aphid species with tested compounds. A significant improvement in aphid performance was observed when sublethal concentrations of Karate and Decis were supplied to aphids through detached leaves. Similar results have been obtained with sublethal concentrations of other toxicants given to wheat aphids as recorded by Mann et al. (1991). Furthermore, our results indicate that the NeemAzal T/S achieved a satisfactory control level on R. padi and M. dirhodum.
Effect of EPNs and Karate on fruit fly
Among EPNs nematodes, in 2009 S. carpocapsae caused the most significant reductions in percent infestation, followed by S. feltiae and H. bacteriophora. While in 2010, S. feltiae and S. carpocapsae had the same efficiency and both were also significantly to H. bacteriophora. This indicated that H. bacteriophora was ineffective under field conditions from the middle of April to the end of May, while S. carpocapsae and S. feltiae were effective at similar temperatures. However, this suggests that the efficacy of EPNs was best evaluated through field trials that embody a broader range of influencing factors than were usually incorporated into bioassays. Also, this may be due to behavioral differences such as mobility and their ability to survive under natural field conditions between the two nematode genera Steinernema and Heterorhabditis as reported in other studies by Molyneux (1985); El-Wakeil and Volkmar (2013).
The damaged-tiller counts were considered as indicators for infestation rates. Treatments applied showed a reduction in O. frit damage relative to the control. These results corresponded with Clements et al. (1985) who stated that synthetic pyrethroids are the most effective chemicals used in controlling O. frit. The percent infestation in Sakha 93 was higher than Triso variety; this may be due to the Triso variety growing faster than the Sakha 93 variety early in the growing season as mentioned by El-Wakeil et al. (2009), El-Wakeil and Volkmar (2013).
Larval mortalities in λ-cyhalothrin treatments and S. carpocapsae were higher than other treatments in 2009; whereas in 2010, S. carpocapsae and S. feltiae achieved the same larval mortality levels and also were still better than H. bacteriophora. This may be due to weather conditions which were warmer and dryer in 2009 than 2010, as confirmed in the other study by El-Wakeil and Volkmar (2011). These results indicate that S. carpocapsae can be used to control O. frit in spring wheat field, because, O. frit begin egg laying in the early to middle part of April. The L2 larvae were found until early May and L3 came in middle to end of May. At that time, temperatures were below the threshold necessary for H. bacteriophora to be an effective biological control agent; therefore efficacy of H. bacteriophora was lower than other EPNs species. The efficacy of S. carpocapsae against O. frit started to increase at 13°C as reported by Gerritsen et al. (1998) in other studies, thus it seems to be better adapted to control insect pests as in case of O. frit. The larval mortality was lower in Triso than Sakha 93 variety; because the percent infestation was also high, therefore it was easily for EPNs to find and parasitize O. frit larvae. These results indicated that these treatments were efficacious on O. frit as alternative control methods.
Effects on the wheat blooms midges
There is a constructive relation between pheromone trap catches and wheat midge infestation (El-Wakeil et al. 2013b). The numbers of orange wheat blossom midge larvae in either water trap types or sticky traps were higher in untreated than treated plots. Karate caused the highest reduction percents, followed by Biscaya, then NeemAzal T/S. The high catches of WBM in the water traps may be attributed to weather conditions, especially rainfall, which had a direct effect and facilitated the migration of midge larvae to the soil. Similar results were recorded in winter wheat by Gaafar (2010), Gaafar et al. (2011) who noted increases in catch densities after heavy rainfall. This is important for crop rotations; insect densities can easily surpass threshold densities if wheat is grown after wheat.
To reduce the economic impact of wheat midges; wheat farmers must be aware of all suitable management strategies. Forecasts and risk warnings, monitoring tools, chemical control, biological control and plant resistance are all available for the industry to manage wheat midges. Although, NeemAzal T/S treatment caused adequate mortality of wheat midges not high as Karate, but it is still safer to the natural enemies (Elliott and Mann 1996; Olfert et al. 2009). Results of water traps is considered as forecasting method for the next year when it intend growing the wheat after wheat.
Effects on wheat insects and the associated natural enemies
Population of aphid, thrips and leafhopper numbers revealed a magnitude changes in treated than untreated plots. Karate achieved a significant reduction of these species than Biscaya and NeemAzal T/S, this result is similar with obtained by Sallam et al. (2009), who mentioned that Karate caused the highest mortality of wheat aphids compared to other compounds. Also, Gaafar and Volkmar (2010) studied effect of Karate for controlling wheat thrips; they found that Karate caused a good reduction percents of thrips populations. Reduction percents of leafhoppers were lower than those of thrips, aphids and bugs; this was due to mobile ability of leafhoppers.
The results indicated that there is a harmful effect of Karate on many natural enemies recorded in the present study. Our results correspond with Croft and Whalon (1982) who studied effects of pyrethroid insecticides against arthropod natural enemies of some agricultural crops. Meena et al. (2002) and Solangi et al. (2007) conducted their experiments using some pyrethroid compounds on coccinellids; they mentioned that the tested insecticides caused reduction percents ranged from 38 to 72% on larval instars. On the other hand, NeemAzal T/S was safer on several of the studied natural enemies as reported by El-Wakeil et al. (2006), who pointed only slight side effect of Neem formulations on lacewings. Also, our findings agree with the results obtained by Kaethner (1991) and Srinivasan and Babu (2000), who reported no deleterious effect of NeemAzal T/s and NeemAzal-F on C. carnea efficacy. Schmutterer (1997) reported in his studies dealing with side effect of neem products on predatory spider and natural enemies that botanic insecticides are safer on different natural enemies as well as insect pathogens.
Natural enemy abundance after two sprays was higher than after one spraying. This may be due to increasing of aphid populations at heading and flowering stages of winter wheat. Many of natural enemy taxa found in this study declined after the insecticide application and the effects were always apparent; there were two groups exhibiting the reaction of natural enemies and their abundance post treatments. Staphylinidae and Syrphidae revealed a moderate decline after spraying; while dance flies and lacewings and were more susceptible after two sprays. Coccinellids were affected moderately by insecticides as confirmed by Swaran (1999); Meena et al. (2002), who found that predatory efficiency of both adult and larvae C. septempunctata was reduced following insecticide application. Generally, there were considerable differences in the insecticide effects on different bio control agent numbers. This is in agreement with several studies for many researchers; Smith and Stratton (1986); Alford et al. (1998); Holland et al. (2000).
The results showed that Karate caused more mortality to wheat insect pests than both Biscaya and NeemAzal T/S. Side effect of Karate was harmful to the natural enemies than other two materials. On the other hand, NeemAzal T/S treatments were safer to the natural enemies. Opportunity to use Biscaya or NeemAzal T/S compatible with parasitoids and predators to control wheat insect pests is tremendously required. Thus, according to their short persistence, Neem formulations or Biscaya with adequate concentrations could be considered the promising active ingredients to use in IPM programs. Sustainable control of wheat insect pests requires careful monitoring and integration of cultural practices and biological controls for wheat production to keep the environment safe and clean.
Our deep thanks are due to Trifoloio for providing us NeemAzal T/S. We are also greatly indebted to Prof. M. Saleh for his helpful comments on the manuscript. This research was supported financially by DFG in Martin Luther University in Halle, Germany.
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