Biology and harmfulness of Brassica pod midge (Dasineura brassicae Winn.) in winter oilseed rape

Draga Graora1*, Ivan Sivčev2, Lazar Sivčev2, Wolfgang Büchs3, Vladimir Tomić4, Boris Dudić4 and Tanja Gotlin Čuljak5 1University of Belgrade, Faculty of Agriculture, Nemanjina 6, 11080 Belgrade, Serbia 2Institute for Plant Protection and Environment, Teodora Drajzera 9, 11000 Belgrade, Serbia 3 Federal Research Centre for Cultivated Plants, Institute for Crop and Soil Science, Bundesallee 50, 38100 Braunschweig, Germany 4University of Belgrade, Faculty of Biology, Studentski trg 3, 11000 Belgrade, Serbia 5 University of Zagreb, Faculty of Agriculture, Svetošimunska cesta 25, 10000 Zagreb, Croatia (*dgraora@agrif.bg.ac.rs) Received: March 17, 2015 Accepted: April 15, 2015


Biology and harmfulness of Brassica pod midge (Dasineura brassicae Winn.) in winter oilseed rape INTrODuCTION
The brassica pod midge (Dasineura brassicae), along with Meligethes aeneus (Fabricius), Ceutorhynchus napi Gyllenhal, C. assimilis Payk., C. pallidactylus (Marsham) and Psylliodes chrysocephala (L.), belongs to a group of most important pests of oilseed rape in Europe . It causes damage primarily to pods of winter wheat and spring oilseed rape, but also to other species in the family Brassicaceae.
Larvae enzymatically dissolve the inner tissue of infested pods (Kazda et al., 2005), causing colour change in the pods, their deformation and cracking, which results in premature seeds dropping. Seed loss of oilseed rape caused by attacks of this species amount to 82% (Williams, 2010).
Over the past thirty-five years of faunistic research in Serbia , D. brassicae has been recorded as a potentially dangerous pest of Brassica oleracea and B. napus in many localities (Simova-Tošić et al., 2000). In recent years, it has been reported in lower numbers in oilseed rape in the Banat region, (Milovanović, 2007).
Our investigation was motivated by different reports on the importance and harmfulness of this species by foreign authors, and by a very insufficient knowledge of this species in Serbia. The purpose of this work was to monitor the life cycle and harmfulness of the brassica pod midge in oilseed rape, and its correlation with the cabbage seed weevil, Ceutorhynchus assimilis Payk.

maTErIaLS aND mETHODS
A survey of D. brassicae was carried out in oilseed rape (Brasica napus L.) in 2011, as well as in winter wheat grown in crop rotation with oilseed rape in 2012. The survey was carried out in the locality Stari Žednik near Subotica, where oilseed rape was grown in a 1.5 ha field. Oilseed rape was sown on September 17, 2010, and harvested on June 22, 2011. The growth stages of winter oilseed rape were determined according to the BBCH scale of Weber & Bleiholder (1990).
In the same field, winter wheat was sown on October 20, 2011 and harvested on June 21, 2012.
Yellow Water Traps (YWT), Syngenta type, were used to detect the emergence of first generation adults of D. brassicae. They were set up in four places in the middle of the field at 50 m distance.
In order to detect the time when larvae leave into the ground to cocoon, funnel traps were installed underneath plants. On each experimental plot, 8 funnel traps were installed at the beginning of the phenophase BBCH 65 and were kept there until harvest. A funnel trap consists of a plastic funnel leading into a plastic dish with 5% sodium benzoate solution (Figure 1). On the experimental plot, 8 emergence traps were also installed at a distance of 50 m, at the beginning of the phenophase BBCH 68 and were kept there until harvest. Emergence traps are tent-shaped with photo-eclectors on top, where insects are collected ( Figure 2). All traps were checked every 7 to 14 days.
Samples were conserved in 70% ethyl alcohol and conveyed to an entomological laboratory to study them under a stereomicroscope.
Pod damage percentage and the number of larvae of D. brassicae per pod were determined by dissection of all pods of the main raceme from 15 plants at the phenophase BBCH 71-73. The percentage of infested pods of both species was calculated using the formula:   Aljmli, 2007). The beginning of immigration of the first generation D. brassicae adults was detected on April 12, when oilseed rape starts flowering (BBCH 60-62). The immigration of adults was rather extended and lasted until the end of May (BBCH 77-78). Both males and females were found in the samples, although some reports had mentioned that only fertilized females immigrated to oilseed rape fields from their overwintering sites (Williams et al., 1987). The long immigration period of first generation imagines, lasting a month and a half, enables very fragile and short-lived midges to find an adequate phenophase of either winter or spring oilseed rape for their development. However, they prefer winter oilseed rape (Axelsen, 1992;Alford et al., 2003). A female lays eggs into pods, where larvae develop. In our investigation, larvae dropped on the ground through cracked pods at the end of their three-week long development. Funnel traps were used to monitor the time when they leave pods, and the number of larvae dropping on the ground (Table 1).
First larvae caught in the funnels were found on May 3 (BBCH 71-73) and their abundance was 13.5 larvae/ m 2 . Their numbers increased in funnels until June 5 (BBCH 79-80), when the maximum of 11116.5 larvae/ m 2 was reached. Over the following period, the number of larvae decreased until June 21 (BBCH 87-88), when the last ones were found in funnels, i.e. all larvae have left pods and reached soil. The pupal stage lasted for about three weeks after which period the emergence of second generation adults was recorded and monitored using photoeclector cages (Table 1).
The beginning of emergence of second generation imagines D. brassicae was recorded on May 26 (BBCH 76-78) when 49.4 larvae/m 2 were found. The highest number of imagines was 177.0/m 2 and it was recorded on June 5 (BBCH 79-80), while the end of emergence was recorded on June 9 (BBCH 81-83) when the weather became hot and dry. The emergence period of the second generation imagines was 14 days.
The number of emerged imagines was found to be much lower than the number of larvae reaching soil. The total number of emerged imagines in tents was 1995.9/ m 2 , or 1.5% of the total number of larvae (131,904.0/m 2 ) in tents. The low number of emerged second generation imagines in the late host phenophase (BBCH 76-78 to BBCH 81-83) did not cause any significant damage to oilseed rape in our survey. In the absence of oilseed rape as a host, larvae of D. brassicae are able to develop in weeds of the cabbage family, and then get into soil to overwinter (Kazda et al., 2005).
Low numbers of emerged second generation adults are likely to be the species' survival strategy under different weather conditions. Emergence of adults may be scarce or completely stop, especially in dry years (Nilsson et al., 2004), as recorded during the warm and dry summer of 2011. Besides, low rates of imagines emergence can be conditioned by possible effects of their natural enemies, both predators (Büchs & Alford, 2003; and parasitoids . Our examination of tents in the summer of 2011, and during the development period of wheat until harvest in the following 2012, showed no flight activity of midges, which indicates that their diapause may last longer than a year, sometimes up to five years (Williams et al., 1987;Alford et al., 2003;Nilsson et al., 2004;Williams & Cook, 2010;Williams, 2010).