Introduction

Sunn Pest, Eurygaster integriceps Puton, is the most important insect pest of wheat in Central and West Asia (Rdjabi 1994; Javahery 1995). Both nymphs and adults of Sunn Pest cause plant damage, feeding on leaves, stems, and grains (Critchely 1998). Yield losses attributable to direct feeding typically range between 50 and 90%, and enzymes injected into the grain during feeding severely compromise the quality of the resulting flour by degrading the vital gluten proteins (Hariri et al. 2000).

The current strategies for Sunn Pest management rely mainly on chemical and cultural controls; in most cases, chemical control is the primary means of management (Miller and Morse 1996). This is a costly and unsustainable means of pest management and has resulted in resistance of Sunn Pest to various types of insecticides (Alexandrescu et al. 1990). Novel management strategies must be investigated for their feasibility for pest management (Parker et al. 2000). Current studies involve the use of resistant wheat varieties, insect pathogens, predators, parasites, and parasitoids (Moore 1998). Among the most promising of these natural controls are the egg parasitoids. Inundative releases of the egg parasitoid Trissolcus grandis (Thomson) in Morocco against a related wheat bug, Aelia germari Kust, at a rate of six parasitoids per bug resulted in >90% egg parasitism and successful wheat bug population suppression (Laraichi and Voegelé 1975). Methods for the rearing of T. grandis on eggs of E. integriceps and an alternative host Graphosoma semipunctata F., a multi-voltine species that can be easily reared in the laboratory, have been determined (Alexandrov 1948; Doğanlar 1998). Studies on the natural occurrence of Sunn Pest egg parasitoids have also been conducted (Zatyamina et al. 1976; Barbulescu 1971; Til`menbaev et al. 1983; Popov et al. 1984, 1987; Kaitazov 1986; Radjabi and Amir-Nazari 1989; Amir-Maafi and Parker 2003), mostly on in-field characterization of their natural impact on Sunn Pest populations. These studies report levels of natural parasitism that sometimes attain 100% (Barbulescu 1971). However, these levels are likely an overestimation biased by late season sampling when the impact of egg parasitoids is of less importance (Amir-Maafi and Parker 2003). By this argument, any inundative or augmented release of egg parasitoids must be done at the initial onset of Sunn Pest oviposition. Prior to any large-scale field release, an estimation of the rate of parasitoids to be prescribed must be conducted. This study investigates the interaction between Sunn Pest and egg parasitoid densities on the resultant percentage of egg parasitism and the quality of the harvested grain.

Materials and methods

In-field evaluation of egg parasitoids

Evaluation of egg parasitoids was made in Al Hassakeh province in Northern Syria. Sampling was conducted from the initial appearance of Sunn Pest eggs until 1 week post-harvest. Three regions were selected, Al Malkia, Al Qameshley and Tall Sheer. In each region, 1 hectare fields were selected and divided into five equally sized subunits. Within each subunit, five 0.25 m2 frames were used and the number of Sunn Pest eggs (parasitized and non-parasitized) were counted and recorded. Evaluations were repeated weekly throughout the growing season.

Determination of the effect of pest and parasitoid densities on the percentage of egg parasitism

Sunn Pest individuals were collected from wheat fields during initial migration from the overwintering sites and transferred to 1 m2 bread wheat plots, variety Cham 6, in screened cages (1×1×1.2 m3) at three densities: two, four, and six Sunn Pest individuals per cage at a 1:1 sex ratio, as a split-plot design with four replicates. The egg parasitoid, T. grandis was even-age reared in the laboratory on field collected E. integriceps eggs at 22±2°C. Adult feeding was supplemented with honey. Two-day-old females were separated from males under a stereoscope and released into the Sunn Pest seeded cages, 3-day post-Sunn Pest release, at three rates: one, two, and three females for each Sunn Pest density. Control plots contained no Sunn Pest, or Sunn Pest at each of the infestation levels without egg parasitoids. Observations of healthy and parasitized egg masses were conducted beginning 1-week post-parasitoid release and continuing until harvest.

Analysis of wheat grain quality

At harvest, the grain from each plot was analyzed for total protein content using the Kjeldahl method (Anonymous 1995). Gluten quality was analyzed using the sodium dodecyl sulphate (SDS) sedimentation method as outlined in Cressey and McStay (1987). Feeding damage caused by Sunn Pest was determined by randomly selecting five sub-samples of 100 grains from each plot and examining them under a stereoscope for the presence of feeding punctures. Grains with at least one puncture site were considered to be damaged.

Impact of Sunn Pest feeding on grain quality for two phenological stages of bread wheat

Two phenological stages of bread wheat variety Cham 6 were exposed to Sunn Pest in meter-square plots as a completely randomized design with four replicates within screened cages (6×9×2 m3). Fifteen insects were added per plot, adults were used for the vegetative wheat stage and fifth instar for the spike stage. After 15 days, the insects were removed and the plants were treated with 0.1% EC50 Decis to kill the remaining insects. Grain quality was assessed using the SDS sedimentation method as previously described.

Results and discussion

In-field evaluation of egg parasitoids

Egg parasitoids were recovered from study sites Al Malkia and Al Qameshly, where the total percent parasitism reached 59 and 22%, respectively. In general, the abundance of parasitized egg masses peaked by the second week of May. This shadowed the maximal abundance of healthy egg masses by 1 week (Fig. 1). No parasitized eggs were recovered from Tall Sheer where chemical insect control against Sunn Pest was conducted on 7 May and 14 May 2003. These results are comparable to those from Iran 1997, 1998 Amir-Maafi and Parker (2003) and reflect their results that the naturally occurring levels of egg parasitism are low during the initial stages of Sunn Pest oviposition. In Al Qameshly and Al Malkia, these rates were 18 and 25%, respectively.

Fig. 1
figure 1

Occurrence of healthy and parasitized Sunn Pest egg masses in Al Malikia, Al Qameshly, and Tall Sheer, Syria, 2003

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Determination of the effect of pest and parasitoid densities on the percentage of egg parasitism

The percent parasitism ranged from 65 to 83% 4-weeks post-exposure when one, two, or three egg parasitoids were present at Sunn Pest densities of two and four insects per square meter (Fig. 2). These values did not differ significantly from each other, indicating that the effect of T. grandis is not dependent on the density of mature egg parasitoids at these densities of Sunn Pest. At six Sunn Pest per square meter, significant differences in the percentage of parasitism were only detectable for the one egg parasitoid per square meter rate; this demonstrated a density-dependence for only the low rate of mature egg parasitoids, indicating that the level of egg parasitism is robust to Sunn Pest densities up to six adults per square meter when challenged with a minimum of two T. grandis per square meter.

Fig. 2
figure 2

Egg parasitism rates for different Sunn Pest densities exposed to one, two, or three mature Trissolcus grandis. Comparisons of the means were made using Fisher’s LSD within Sunn Pest density group. Means superscripted with the same letter are not significantly different at the α=0.05 level of significance

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Analysis of wheat grain quality

In general, gluten quality was significantly better and comparable to non-Sunn Pest infested wheat, when one, two, or three egg parasitoids were present at Sunn Pest densities of 2 and 4 insects per square meter (Fig. 3). At six Sunn Pest per square meter, the same effect was found for levels of two and three egg parasitoids per square meter, while the SDS sedimentation value was significantly lower than the control wheat plot, at the six Sunn Pest per square meter density challenged with only one mature egg parasitoid. These results were similar to the results from the effect of mature egg parasitoid and Sunn Pest densities on the rate of egg parasitism, indicating an association between the percentage of egg parasitism and the actualized bread wheat grain quality.

Fig. 3
figure 3

Sedimentation analysis of gluten quality for bread wheat plots (variety Cham 6) infested with three densities of Sunn Pest and challenged with three densities of egg parasitoids. Mean values superscripted with the same letter within a given Sunn Pest density are not significantly different at the α=0.05 level of significance using Fisher’s LSD. The horizontal dashed line indicates the average sedimentation value for the control wheat cages without Sunn Pest and without egg parasitoids

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Impact of Sunn Pest feeding on grain quality for two phenological stages of bread wheat

In general, the level of protein obtained from all Sunn Pest infested and non-infested plots were the same (Table 1). Analysis of the quality of these proteins, using the SDS sedimentation method, showed that the grain was acceptable for baking purposes for only the control and the vegetative stage insect-challenged plots.

Table 1 Grain quality characteristics for bread wheat variety Cham 6 challenged for 2 weeks with 15 Sunn Pest per square meter
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No Sunn Pest feeding damage was observed in the grain harvested from the vegetative-stage insect-challenged plots. The sedimentation value was also comparable to that of the control grains. More than two-thirds of the grains from the spike-stage insect-challenged plots exhibited Sunn Pest feeding damage, and the sedimentation value was nearly 60 ml less than that of the control plots. A decrease in sedimentation greater than 20 ml is considered an indication of bug damage (Cressey and McStay 1987). This wheat is not suitable for baking purposes even though the total protein content is statistically identical to the other treatment. These data show that the impact of Sunn Pest feeding on the quality of bread wheat grain is not actualized before the spike stage.

Overall, these results suggest that any augmented use of T. grandis for management of E. integriceps needs to be initiated after the first observance of E. integriceps eggs in the field, as the occurrence of parasitized eggs was observed within 1 week of the appearance of healthy eggs. During this time the parasitoids would be developing within the eggs. Any management tactic that requires weeks of time for efficacy is dependent on the ability of the host crop to sustain the target pest’s impact until meaningful efficacy is achieved. As there was no impact of vegetative-stage feeding of E. integriceps on the baking quality of the resultant flour from the grain of the same plants, the vegetative stage of wheat represents a time period where the use of chemical insecticides could be used with restraint to allow for an augmented release of T. grandis to demonstrate efficacy. As shown by the in-field characterization of E. integriceps egg parasitism, the ratio of parasitized versus healthy egg masses increases throughout the season in the absence of a chemical insecticide application, suggesting that a one-time mass-release of T. grandis would be more cost-effective than interval small-scale releases.