Agricultural and Food Science, Vol. 15 (2006): 61–72. 61 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Vol. 15 (2006): 61–72. © Agricultural and Food Science Manuscript received February 2005 Insect pests and their natural enemies on spring  oilseed rape in Estonia: impact of cropping systems Eve Veromann, Tiiu Tarang, Reelika Kevväi, Anne Luik Institute of Plant Protection, Estonian Agricultural University; Kreutzwaldi 64, Tartu 51 014, Estonia, e-mail: eve.veromann@loodusfoto.ee Ingrid Williams Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, United Kingdom To investigate the impact of different cropping systems, the pests, their hymenopteran parasitoids and predatory ground beetles present in two spring rape crops in Estonia, in 2003, were compared. One crop was grown under a standard (STN) cropping system and the other under a minimised (MIN) system. The STN system plants had more flowers than those in the MIN system, and these attracted significantly more Meligethes aeneus, the only abundant and real pest in Estonia. Meligethes aeneus had two population peaks: the first during opening of the first flowers and the second, the new generation, during ripening of the pods. The number of new generation M. aeneus was almost four times greater in the STN than in the MIN crop. More carabids were caught in the MIN than in STN crop. The maximum abundance of carabids occurred two weeks before that of the new generation of M. aeneus, at the time when M. aeneus larvae were dropping to the soil for pupation and hence were vulnerable to predation by carabids. Key words: spring oilseed rape, pollen beetles, Hymenoptera, Carabidae Introduction In Estonia, the cultivation of oilseed rape (Brassi- ca napus L., Brassica rapa L.) has expanded great- ly in recent years and now exceeds 46,300 ha (Sta- tistics Board 2003). This provides good potential for population growth of crucifer-specialist, phy- tophagous pests. In Europe, the most common pests of oilseed rape are Meligethes aeneus (Fab.), Meligethes viridescens (Fab.) (pollen beetles), Ceutorhynchus assimilis (Payk.) (cabbage seed weevil), Ceutorhynchus pallidactylus (Marsham) (cabbage stem weevil), Ceutorynchus napi Gyll. (rape stem weevil), Dasineura brassicae (Winn.) (brassica pod midge), Psylliodes chrysocephala (L.)(cabbage stem flea beetle) and Phyllotreta nemorum (L.), Phyllotreta undulata (L.) and Phyl- 62 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Veromann, E. et al. Oilseed rape insects in Estonia lotreta diademata (L.) (flea beetles) (Alford et al. 2003). The management of pests on oilseed rape throughout Europe still relies heavily on chemical pesticides, most often applied routinely and pro- phylactically, often without regard to pest inci- dence (Williams 2004). This leads to the over-use of pesticides, which reduces the economic com- petitiveness of the crop and threatens biological diversity. The pesticides also kill the natural agents of biological control, which would be a natural re- source of great potential benefit to the farmer and the consumer (Alford et al. 1995, Williams and Murchie 1995). By killing natural enemies, pesti- cide applications must be increased further to achieve pest control (Pickett et al. 1995, Murchie et al. 1997). Parasitoids can control the pests. For example, more than 30 species of hymenopterous parasitoids have been reported to attack C. assimi- lis in Europe (Williams 2003). Of these, the larval ectoparasitoid Trichomalus perfectus Walker (Hy- menoptera: Pteromalidae) is widely distributed and particularly important (Lerin 1987, Murchie and Williams 1998a). In addition to killing larvae through direct parasitism, it further kills by host feeding, and reduces damage to infested pods by preventing host larvae from eating their full com- plement of seeds (Murchie and Williams 1998b). Host selection by parasitoids may be influenced by plant characteristics (Vinson 1976) and plant ar- chitecture may alter parasitoid searching efficiency (Billqvist and Ekbom 2001a,b). Unlike parasitoids, predators are usually non- specific and their attacks on pests within oilseed rape crops tend to be fortuitous rather than targeted (Büchs 2003a). In oilseed rape fields, the dominant predators are carabids, these having the greatest biomass in comparison with rove beetles and spi- ders (Goltermann 1994). They are present all year round and can suppress pest populations at an ear- ly stage (Büchs 2003a). Over 20 species of carabid occur regularly in European oilseed rape fields. The species’ composition within communities var- ies from country to country and also from site to site, according to regional or local conditions; changes have also occurred over time, with larger species (e.g. Carabus spp.) being less abundant now than formerly. The occurrence of carabids is greatly influenced by the farming system, being greater in extensively-managed than in intensive- ly-managed crops (Hokkanen and Holopainen 1986, Büchs 2003b). Recent advances in the management of oilseed rape pests have emphasised the important role of natural enemies within integrated pest manage- ment systems for the crop (Williams 2004). The EU-funded project MASTER: MAnagement STrategies for European Rape pests aims to de- velop economically-viable and environmentally- acceptable crop management strategies for winter oilseed rape which maximise the biological con- trol of key pests and minimise chemical inputs (Williams et al. 2002). This requires much greater knowledge of pest, parasitoid and predator taxon- omy and biology throughout Europe. In Estonian conditions, the pests of oilseed rape and their natu- ral enemies have been little studied. The present pilot study aims to add to knowledge of rape pests and their natural enemies in Estonia and contrib- utes to the project MASTER. The aim of this pilot study was to compare the effects of minimised (no plough, direct drilling, no pesticides) and standard (plough, standard applica- tion of pesticides) cropping systems on oilseed rape plant architecture and the occurrence of pests, their hymenopteran parasitoids and carabid preda- tors. Material and methods The study site The study compared a minimised (MIN) with a standard (STN) system of cropping spring oilseed rape in 2003. The study site comprised two adja- cent, approximately rectangular fields (both 2 ha) on Pilsu Farm, Tartu County, Estonia (58°14´ lati- tude 26°16´ longitude). The soil was loamy (aver- age pH KCI 6.15). In both fields, spring oilseed rape cv. Quantum (seeding rate 6 kg ha-1) was drilled on 12 May, following winter wheat. 63 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Vol. 15 (2006): 61–72. In the STN system, ploughing and pesticides were used. The herbicide Treflan Super (2 l ha-1) was applied before drilling, and the herbicide Lontrel 300 (0.3 l ha-1) was applied at the two-leaf growth stage (BBCH-stage) (BBCH 12 of Meier (2001), Lancashire et al. (1991)). The fungicide Folicur (1 l ha-1) was applied at BBCH 50–51 and the insecticide Fastac (0.15 l ha-1) at BBCH 65–66. In the MIN system, direct drilling replaced plough- ing and no pesticides were used. The fields were bordered to the north by an as- phalt road, with a 10 m strip of barley between the road and the oilseed rape, to the south by winter wheat, to the west by grassland and to the east by a crop of barley. The MIN field had many weeds, dominated by Tripleurospermum inodorum (L.), Stellaria media (L.) and Galeopsis tetrahit L. In the STN field, Capsella bursa-pastoris (L.) was abundant. In 2003, spring/summer weather was warmer and wetter than average. Data from the local mete- orological station at Eerika, near Tartu showed that May temperatures (mean 11.6°C) were 1.4°C and July temperatures (mean 19.4°C) were 1.5°C warmer than the long-term average. Rainfall in May (mean 142.8 mm) was 2.3 times greater, and in August (mean 132.8 mm) almost 2 times greater than the long term average. The warm, moist spring promoted the growth and development of the rape crop whereas the wet August inhibited crop ripening and harvesting. Insect sampling Insects were sampled using water and pitfall traps emptied weekly from post-drilling (14 May) to pre- harvest (27 August). The water traps (4 in STN and 4 in MIN), consisted of yellow plastic bowls (210 × 310 × 90 mm), each containing about 1.5 l water. They were positioned at the top of the crop canopy to sample flying insects and raised weekly, as nec- essary, to keep pace with crop growth. Four were placed within the crop 15 m from different borders and two were placed outwith the crop. Pitfall traps for sampling carabids were placed along a central transect of each field (5 in STN and 5 in MIN). Insect samples were sorted and target taxa identified and counted in the laboratory. The cruci- fer-specialists, hymenopterous parasitoids and ground beetles were separated and stored in 70% ethanol at –18°C. The target phytophagous insects and carabids were identified to species. Hymenop- terous parasitoids were identified to family, except those specialised on the target phytophagous in- sects, which were identified to species. Plant sampling The growth stages of the rape plants in both crops were recorded weekly using the Meier (2001) key. Plant density, architecture and infestation and damage by pests were also determined in both crops. Oilseed rape plant and weed density per m2 was determined from 5 randomly-selected places in both fields on two occasions (BBCH 12 and 69–71). Plant architecture and pest infestation was determined on 10 plants from 5 randomly-chosen locations (50 plants from STN and 50 from MIN) collected on 21 August (BBCH 83). Each plant was measured (stem height and diameter and the number of pods and podless stalks on the main ra- ceme and side branches). Damage caused by M. aeneus was assessed as the number of podless stalks (podless stalks in the very top of the stem were not counted because this may have been caused by other factors, e.g. lack of pollination). Stems were dissected for C. pallidactylus larval mining damage. Pods were examined for the pres- ence of live or dead C. assimilis and D. brassicae larvae, the exit holes of emerged C. assimilis lar- vae or those of its ectoparasitoids or pod shatter due to D. brassicae larvae. Statistical analysis Although only one field with each cropping sys- tem was observed the data were analysed using the following statistical methods because all other conditions in the two fields were similar. Statistical analysis used SAS GLM and GENMOD proce- dures. The differences of means of plant parame- 64 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Veromann, E. et al. Oilseed rape insects in Estonia ters and the numbers of oilseed rape and weed plants per m2 were compared with analysis of vari- ance. Comparisons of the numbers of pests, parasi- toids and carabids were made using type 3 empiri- cal standard errors analysis and the Poisson distri- bution and the log link function. The numbers of pests and carabids caught each week were also analysed separately. For analyses of the numbers of carabids the scale parameter was estimated by Pearson’s Chi-Square divided by the degrees of freedom because of overdispersion of the model. Results Plant density, architecture and   pest damage Plant density was similar in both crops, early in development (BBCH 12; MIN, mean 86.3 per m2; STN, mean 91.3 per m2), as well as later, (BBCH 69–71), however, there were significantly more weeds in the MIN field (P = 0.0015) (Fig. 1). The dominating weed was T. inodorum. Stem height, stem diameter and the number of side branches were similar in the MIN and the STN crop. However, main raceme and side branch- es of the MIN plants had significantly (P = 0.043 and P = 0.0016) fewer pods than those of the STN plants (Fig. 2). Damage by M. aeneus, assessed as podless stalks, was less in the STN than in the MIN field (Fig. 2). Few pods were damaged by C. assi- milis and damage was similar between treatments (1% of 4208 dissected pods from STN field and 0.5% of 2740 dissected pods from MIN field). No infestation by D. brassicae was found. Fig. 1. The median number of oilseed rape plants (BBCH 69–71) and weeds per m2 in standard (STN) and minimised cropping system (MIN) fields on Pilsu Farm, Tartu Coun- ty, Estonia in 2003. Fig. 2. The median number of podless stalks on the main raceme, of pods on the main raceme and on side branches on rape plants grown using a standard cropping system (STN) and a minimised cropping system (MIN) on Pilsu Farm, Tartu County, Estonia, in 2003. Min, max 25%, 75% Oilseed rape Weeds MedianNo in m 2 -40 40 120 200 280 360 STN MIN ANOVA: Weeds: F(1,8)=22, P=0.0015 Oilseed rape: F(1,8)=1.86, P=0.21 N=5 Pods on main raceme Podless stalks Pods on side branch Median; Box: 25%, 75%; Whisker: Min, Max -20 20 60 100 140 180 220 260 STN MIN No ANOVA: Main raceme: F(1,98)=4.19, P=0.043 Side branches: F(1,98)=10.6, P=0.0016 Podless stalks: F(1,98)=15.93, P=0.00013 N=50 65 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Vol. 15 (2006): 61–72. Pest incidence and phenology During the study, 60 samples with a total of 2,588 specimens of crucifer-specialist insect pests from eight taxa (Table 1) were collected from the water traps (MIN, 792 specimens; STN 1,796 speci- mens). Meligethes aeneus started to colonise the oilseed rape from BBCH 12 (Fig. 3), increasing from 12 June (BBCH 14) and showing two popu- lation peaks, on 2 July and 13 August. The first peak coincided with first flower (BBCH 59–60). The second occurred during pod ripening (BBCH 80–81). At both peaks and throughout the study period, M. aeneus abundance was greater in the STN field than in the MIN field (Fig. 4, χ² = 11.04, df = 1, P = 0.0009). Ceutorhynchus assimilis abundance was low on both crops (Fig. 4). The first were found on 12 June (BBCH 14). There were two population Table 1. The species’ composition and the mean number of crucifer-specialists caught in yellow water traps (4 per system, N = 60) in spring oilseed rape grown using a standard and a minimised cropping system on Pilsu Farm, Tartu County, Estonia, in 2003. Species Cropping system P value Minimised Standard Mean Std. dev Mean Std. dev Meligethes aeneus 11.83 17.44 25.60 53.26 P < 0.0009 Meligethes viridescens 0.42 1.01 0.63 1.06 Ceutorhynchus assimilis 0.27 0.58 0.85 1.79 P < 0.0001 Ceutorhyncuhs rapae 0.23 0.67 1.43 4.48 P < 0.0001 Ceutorhynchus floralis 0.03 0.18 0.02 0.13 Ceutorhynchus pallidactylus 0.00 0.00 0.02 0.13 Ceutorhynchus pleurostigma 0.02 0.13 0.00 0.00 Phyllotreta 0.40 1.64 1.32 3.68 Fig. 3. The median numbers of Meligethes aeneus per yellow water trap caught at different growth stages (BBCH) in stand- ard (STN) and minimised (MIN) cropping system fields of spring oilseed rape on the Pilsu Farm, Tartu County, Estonia, in 2003 (* indicates significant difference between systems). STN MIN Median; Box: 25%, 75%; Whisker: Min, Max BBCH/Date -50 0 50 100 150 200 250 300 350 400 0/ 21 .0 5 10 /2 8. 05 12 /0 4. 06 14 /1 1. 06 30 -3 1/ 18 .0 6 50 -5 1/ 25 .0 6 59 -6 0/ 02 .0 7 63 -6 5/ 09 .0 7 65 -6 6/ 16 .0 7 69 -7 1/ 23 .0 7 79 -8 0/ 30 .0 7 80 /0 6. 08 80 -8 1/ 13 .0 8 82 -8 3/ 20 .0 8 87 -8 9/ 27 .0 8 No * ** *N = 4 66 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Veromann, E. et al. Oilseed rape insects in Estonia peaks, the first at first flower (BBCH 59–60) and the second during pod maturation (BBCH 79–80). Abundance was greater in the STN field than in the MIN field (Fig. 5, χ² = 26.02, df = 1, P < 0.0001). Parasitoid incidence and phenology Hymenopteran parasitoids from six superfamilies and 18 families were captured in the water traps (MIN, 828 specimens; STN, 660 specimens). Amongst them were four parasitoids of M. aeneus: Diospilus capito, Phradis morionellus, Phradis in- terstitialis and Tersilochus heterocerus and two parasitoids of C. assimilis: Mesopolobus morys and T. perfectus (Table 2). The number of parasitoids increased as the rape started to flower (BBCH 59–60). At full flow- er, numbers were greater in the STN than in MIN field (Fig. 5). The parasitoid population reached maximum during pod ripening (BBCH 79–80) in the MIN field. The numbers of key parasitoids caught from the two cropping systems were simi- lar and not large. Of the M. aeneus endoparasi- toids, D. capito, P. morionellus, P. interstitialis and T. heterocerus, totals of 47 and 51 specimens were found in the STN and the MIN field, respectively. Of the C. assimilis parasitoids, M. morys and T. perfectus, only one specimen was found in STN field and 3 specimens in MIN field. Peak abun- dance of D. capito, the endoparasitoid of M. ae- neus larvae, coincided with peak abundance of new generation M. aeneus (BBCH 80–83). Peak abundance of P. morionellus, P. interstitialis and T. heterocerus, coincided with M. aeneus colonisa- tion. A total of only three specimens of T. perfec- tus, and one specimen of M. morys, both ectopara- sitoids of C. assimilis larvae, were found. Carabid incidence and phenology During the study, 150 pitfall trap samples were collected, containing a total of 3,045 carabids. Ac- tivity-density was greater in the MIN than in the STN field (from MIN 2169 and STN 876 speci- mens; χ² = 6.27; df = 1; P = 0.0123) (Table 3). In the MIN field, maximal activity-density of cara- Fig. 4. The median numbers of Ceutorhynchus assimilis per yel- low water trap caught at different rape growth stages (BBCH) in standard (STN) and minimised (MIN) cropping systems fields of spring oilseed rape on Pilsu Farm, Tartu County, Estonia, in 2003 (* indicates significant difference between systems). STN MIN Median; Box: 25%, 75%; Whisker: Min, Max BBCH/Date No -1 1 3 5 7 9 0/ 21 .0 5 10 /2 8. 05 12 /0 4. 06 14 /1 1. 06 30 -3 1/ 18 .0 6 50 -5 1/ 25 .0 6 59 -6 0/ 02 .0 7 63 -6 5/ 09 .0 7 65 -6 6/ 16 .0 7 69 -7 1/ 23 .0 7 79 -8 0/ 30 .0 7 80 /0 6. 08 80 -8 1/ 13 .0 8 82 -8 3/ 20 .0 8 87 -8 9/ 27 .0 8 * * * N = 4 67 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Vol. 15 (2006): 61–72. Table 2. Total numbers of hymenopteran parasitoids caught in yellow water traps (4 per system) in standard and minimised cropping system fields of spring oilseed rape on Pilsu Farm, Tartu County, Estonia, in 2003. Superfamily Family/Species Standard Minimised Chalcidoidea Eulophidae 32 55 Eurytomidae 15 9 Pteromalidae 163 344 Trichomalus perfectus (Walker) 1 2 Mesopolobus morys (Walker) 0 1 Mymaridae 25 16 Encyrtidae 41 35 Eupelmidae 1 1 Trichogramatidae 0 1 Platygastroidea Platygastridae 83 65 Scelionidae 43 40 Ichnemonoidea Braconidae 34 61 Diospilus capito (Nees) 6 1 Ichnemonidae 60 65 Tersilochus tripartitus (Brischke) 1 3 Tersilochus heterocerus Thomson 0 1 Phradis morionellus (Holmgren) 22 42 Phradis interstitialis (Thomson) 19 7 Cerphronoidea Megaspilidae 3 4 Ceraphronidae 100 56 Proctotrupoidea Proctotrupidae 3 2 Diapriidae 1 9 Cynipoidea Eucoilidae 6 6 Cynipidae 0 2 Figitidae 1 0 Total 660 828 Fig. 5. The median numbers of hymenopteran parasitoids per yellow water trap caught at dif- ferent rape growth stages (BBCH) in standard (STN) and minimised (MIN) cropping system fields of spring oilseed rape on the Pilsu Farm, Tartu County, Estonia, in 2003. STN MIN Median; Box: 25%, 75%; Whisker: Min, Max BBCH/Date No -20 0 20 40 60 80 120 140 160 0/ 21 .0 5 10 /2 8. 05 12 /0 4. 06 14 /1 1. 06 30 -3 1/ 18 .0 6 50 -5 1/ 25 .0 6 59 -6 0/ 02 .0 7 63 -6 5/ 09 .0 7 65 -6 6/ 16 .0 7 69 -7 1/ 23 .0 7 79 -8 0/ 30 .0 7 80 /0 6. 08 80 -8 1/ 13 .0 8 82 -8 3/ 20 .0 8 87 -8 9/ 27 .0 8 N=4 100 68 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Veromann, E. et al. Oilseed rape insects in Estonia Table 3. The species composition and mean number of carabids caught with pitfall traps (5 per system, N = 75) in standard and minimised cropping system fields of spring oilseed rape on Pilsu Farm, Tartu County, Estonia, in 2003. Species Cropping system P < 0.05 Standard Minimised Mean Std dev Mean Std dev Pseudoophonus rufipes (Degeer) 16.64 29.81 6.33 8.80 * Harpalus affinis (Schrank) 0.20 0.44 0.16 0.49 Poecilus cupreus (Linnaeus) 5.39 11.94 1.91 3.06 * Pterostichus melanarius (Illiger) 3.72 5.15 0.69 1.39 * Pterostichus niger (Schaller) 0.60 1.38 0.07 0.30 Agonum muelleri (Herbst) 0.85 1.92 0.19 0.67 Anchomenus dorsalis (Pontoppidan) 0.32 0.89 0.47 1.55 Clivina fossor (Linnaeus) 0.19 0.46 0.15 0.39 Calathus melanocephalus (Linnaeus) 0.03 0.16 0.59 3.60 Amara aulica (Panzer) 0.28 1.20 0.03 0.16 Amara spp 0.01 0.12 0.00 0.00 Amara fulva (Müller) 0.01 0.12 0.03 0.16 Amara bifrons (Gyllenhal) 0.11 0.45 0.20 0.66 Carabus cancellatus (Illiger) 0.05 0.23 0.08 0.27 Bembidion properans (Stephens) 0.37 0.82 0.51 1.01 Bembidion quadrimaculatum (Linnaeus) 0.00 0.00 0.03 0.16 Bembidion lampros (Herbst) 0.11 0.35 0.05 0.23 Acupalpus meridianus ( Linnaeus) 0.00 0.00 0.01 0.12 Calathus erratus (Sahlberg) 0.03 0.16 0.19 0.59 Asaphidion pallipes (Duftschmid) 0.01 0.12 0.01 0.12 bids was reached at the end of rape flowering (BBCH 69) (Fig. 6). The three most abundant spe- cies in both the MIN and the STN fields were Pseudoophonus rufipes, Poecilus cupreus and Pterostichus melanarius. Pseudoophonus rufipes was the dominant carabid species caught, consti- tuting more than half of all specimens in both fields. Poecilus cupreus was the second most abun- dant species. Both of them were caught signifi- cantly more in the MIN than in the STN field (P. rufipes: χ² = 5.71; df = 1; P = 0.0169; P. cupreus: χ² = 5.90; df = 1; P = 0.0151) and their activity- density peak coincided with M. aeneus larval drop at the end of rape flowering (BBCH 69) (Fig. 6). Discussion During the study, the three major European pests of oilseed rape: M. aeneus, C. assimilis and C. pal- lidactylus (one specimen only) were collected. Meligethes aeneus was by far the most numerous and the only one to reach pest status. The second most abundant pest was C. assimilis. A few M. viridescens were also caught; this species requires higher temperatures for oviposition and develop- ment than M. aeneus (Alford et al. 2003). In addi- tion, Ceutorhynchus rapae, C. floralis, C. pleu- rostigma and flea beetles (Phyllotreta spp.) were also captured but their abundance was low. Ceuto- rhynchus rapae is infrequently recorded in Estonia (Metspalu and Hiiesaar 2002) and therefore the relative large number caught (totally 50, in BBCH 12 in STN field) was unusual. Insect incidence on oilseed rape is dependent on several factors, such as oilseed rape plant architecture, presence of flowering weeds, crop rotations, landscape struc- ture etc. (Walters et al. 2003). Weeds can exert di- rect stress on crops (by competing for sunlight, moisture etc.) or affect indirectly through enhanc- ing the presence of the natural enemies of pests (Altieri and Nicholls 2004). In our study, oilseed rape plant density was similar in both crops but there were significantly more weeds in the MIN 69 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Vol. 15 (2006): 61–72. Fig. 6. The median numbers of carabids per pitfall trap caught at different rape growth stages (BBCH) in standard (STN) and minimised (MIN) cropping sys- tem fields of spring oilseed rape on Pilsu Farm, Tartu County, Es- tonia, in 2003 (* indicates signifi- cant difference between sys- tems). field. The weeds were large enough to compete with the crop plants for food and light, probably accounting for the reduction in the number of flow- ers on the side branches of the rape plants in the MIN compared with the STN field. The greater abundance of rape flowers in the STN field pro- vided a greater food resource for M. aeneus so their damage to the main raceme was lower in the STN than in the MIN field, where the beetles con- centrated on the main raceme on the plants. The two most numerous pests, M. aeneus and C. assimilis, each had two population peaks at ap- proximately the same time, the first at first flower (BBCH 59–60) and the second during pod ripen- ing (BBCH 80–81). The second peak indicated emergence of the new generation from the soil. Despite the application of insecticide to the STN field at BBCH 65 pest abundance was greater in the STN field than in the MIN field throughout the study period. This could be explained by differ- ences in crop performance in the case of M. ae- neus, and in the case of C. assimilis, by the greater resource of young pods for oviposition. The crop- ping system appears to have influenced rape plant architecture, enabling plants in the STN field to produce more flowers than those in the MIN field, which in turn resulted in greater infestation by M. aeneus and C. assimilis in the former. Parasitoids of both of key pests were found. Four parasitoids of M. aeneus: D. capito, P. mori- onellus, P. interstitialis and T. heterocerus and two parasitoids of C. assimilis: M. morys and T. perfec- tus were captured. All are recorded for the first time in Estonia (Tryapitzyn 1978, Kasparjan 1981). These parasitoid species are found over most of Europe, from southern Sweden to France (Nilsson 2003, Williams 2003) with those of M. aeneus at the northern distribution limit of oilseed rape in Finland (Hokkanen 1989). The distribution and abundance of different species depends on fac- tors such as the local climate, the crops grown dur- ing previous years and the cultivation techniques used (Nilsson 2003). At full flower, the number of parasitoids was greater in the STN than in MIN field, probably attracted by the greater abundance of flowers; adult parasitoids are exclusively de- pendent on floral and extrafloral nectar, honeydew and pollen for food (Lewis et al. 1998). During STN MIN Median; Box: 25%, 75%; Whisker: Min, Max BBCH/Date No -20 20 60 100 140 180 220 260 0/ 21 .0 5 10 /2 8. 05 12 /0 4. 06 14 /1 1. 06 30 -3 1/ 18 .0 6 50 -5 1/ 25 .0 6 59 -6 0/ 02 .0 7 63 -6 5/ 09 .0 7 65 -6 6/ 16 .0 7 69 -7 1/ 23 .0 7 79 -8 0/ 30 .0 7 80 /0 6. 08 80 -8 1/ 13 .0 8 82 -8 3/ 20 .0 8 87 -8 9/ 27 .0 8 N=5 70 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Veromann, E. et al. Oilseed rape insects in Estonia pod ripening (BBCH 79–80), the further increase in the number of parasitoids in the MIN field prob- ably indicated the emergence of new generations of some hymenopteran parasitoid species. Key parasitoid phenology was synchronised with that of their hosts. Peak abundance of D. capito, coin- cided with peak abundance of new generation M. aeneus (BBCH 80–83), indicating that they prob- ably emerged from host larvae in the oilseed rape. Diospilus capito is multivoltine with two or three generations in northern Europe (Billquist and Ek- bom 2001a, Nilsson 2003). The other captured parasitoids of M. aeneus have one generation per year and after pupating in the host pupal chamber in the soil stay in diapause in the cocoon until the following spring or summer (Nilsson 2003); they were found at the same time as M. aeneus colo- nised. Due to the low abundance of C. assimilis a very few of its parasitoids were found also. Tri- chomalus perfectus is a univoltine ectoparasitoid reported, in winter rape, to have an abundance peak two to four weeks after peak migration of C. assimilis into the crop. New-generation parasitoids mate on emergence and leave the crop shortly be- fore harvest. Only females overwinter, possibly in evergreen foliage (Williams 2003). In Estonia, the total number of key parasitoids was very low prob- ably because the history of oilseed cropping is short and the parasitoids may need more time to build up their populations. Although their greater abundance in the MIN field suggests potential to encourage them with more environmentally- friendly crop management, but this requires addi- tional research. Beside parasitoids, carabids also have potential to impact rape pest populations through predation. For example, fully-grown larvae of M. aeneus, drop to the ground for pupation, and are then im- portant components of the diet of carabids (Büchs and Alford 2003). The MIN field had greater abun- dance of carabids than the STN field. This agrees with the findings of Hokkanen and Holopainen (1986), Langmaack et al. 2001 and Irmler (2003) who also found more individuals and species of carabids on biologically- or minimally-managed fields, which they ascribed to the availability of more prey. Also Altieri and Nicholls (2004) high- lighted the important role of weeds in the presence of predators in the fields. This could be true also for the present study, where the MIN field with its reduced tillage, no pesticides and more weeds of- fered greater food resources for carabids. Maximal activity-density of carabids in the MIN field was two weeks before the maximal abundance of the new generation of M. aeneus. This is the period when M. aeneus larvae are mature, drop to the soil to pupate, and are most vulnerable to predation. The three most abundant species in both fields: P. rufipes, P. cupreus and P. melanarius have been reported as typical of winter rape fauna (Lang- maack et al. 2001, Luik et al. 2001). According to Thiele (1977), 50% of the food consumed by P. rufipes is animal matter. Poecilus cupreus is an im- portant predator of M. aeneus larvae (Büch 2002). Similarily to our data, Büchs and Nuss (2000) also found strong coincidence between the time of the occurrence of P. cupreus and P. melanarius and that of oilseed rape pest larvae during their change of strata for metamorphosis, and suggested that carabids are important larval predators. Predatory efficacy is greatly influenced by the time period over which carabids can prey upon M. aeneus lar- vae. With unlimited access to the larvae during the whole “dropping” period, mortality of larvae can be considerable (78%) (Büchs 2003a). Delayed flowering of the crop, high density of pest larvae and longer duration of the larval “dropping” period enhances the positive effects of polyphagous epi- gaeic predators in oilseed rape (Büchs 2003a). Al- though there was more potential prey (M. aeneus larvae) in the STN field, there were significantly fewer carabids in the STN than in the MIN field. This was probably caused by insecticide treatment, to which carabids are known to be sensitive. Tuu- bel and Toom (1999) found that the treatment of a barley field with Fastac significantly decreased the numbers of Harpalus and Pterostichus. The appli- cation of Fastac to the STN field (BBCH 65–66) probably killed a proportion of the carabids either directly or via poisoned prey. Therefore activity- density peak of carabids was obvious only in the MIN field, where their pressure on M. aeneus lar- vae was stronger. Thus, in the MIN system, the reduced abundance of new generation M. aeneus 71 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Vol. 15 (2006): 61–72. and C. assimilis could have resulted from both the lower number of rape flowers and the greater mor- tality of pest larvae from the more abundant para- sitoids and predators. Acknowledgements. We thank Marge and Madis Ajaots, Pilsu Farm, for crop husbandry and two anonymous re- viewers for constructive comments. This study was sup- ported by the EU Framework 5 project MASTER: Inte- grated pest management strategies incorporating bio-con- trol for European oilseed rape pests (QLK5-CT-2001- 01447) and Estonian Science Foundation grants Nr 5736 and 4993. Rothamsted Research receives grant-aided sup- port from the UK Biotechnology and Biological Sciences Research Council. References Alford, D.V., Murchie, A.K. & Williams, I.H. 1995. Observa- tions on the impact of standard insecticide treatments on Trichomalus perfectus, a parasitoid of seed weevil on oilseed rape in the UK. Bulletin IOBC wprs 18, 4: 122–126. Alford, D.V., Nilsson, C. & Ulber, B. 2003. Insect pest of oilseed rape crops. In: Alford, D.A. (ed.). Biocontrol of oilseed rape pests. Oxford, UK: Blackwell Science Ltd. p. 10–41. Altieri, M.A. & Nicholls, C.I. 2004. Biodiversity and pest management in agroecosystems. 2nd ed. Food Prod- ucts Press. 236 p. Billqvist, A. & Ekbom, B. 2001a. Effects of host plant spe- cies on the interaction between the parasitic wasp Diospilus capito and pollen beetles (Meligethes spp.). Agricultural and Forest Entomology 3: 147–152. Billqvist, A. & Ekbom, B. 2001b. The influence of host plant species on the parasitism of pollen beetles (Meligethes spp.) by Phradis morionellus. Entomologia Experimen- talis et Applicata 98: 41–47. Büch, R. 2002. Mortality of pollen beetle (Meligethes spp.) larvae due to predators and parasitoids in rape fields and the effect of conservation strips. Agriculture, Eco- systems and Environment 90: 225–263. Büchs, W. 2003a. Predators as biocontrol agents of oilseed rape pests. In: Alford, D.A. (ed.). Biocontrol of oilseed rape pests. Oxford, UK: Blackwell Science Ltd. p. 279– 298. Büchs, W. 2003b. Impact of on-farm landscape structures and farming systems on predators. In: Alford, D.A. (ed.). Biocontrol of oilseed rape pests. Oxford, UK: Blackwell Science Ltd. p. 245–227. Büchs, W. & Nuss, H. 2000. First steps to assess the impor- tance of epigaeic active polyphagous predators on oilseed rape insects pests with soil pupating larvae. Bulletin IOBC wprs 23, 6: 151–163. Goltermann, S. 1994. Das auftreten von laufkäfern (Col. Carabidae) auf winterrapsfeldern und deren einfluss auf den massenwechsel von Meligethes aeneus F. (Col. Nitulidae). PhD thesis, University of Rostock,PhD thesis, University of Rostock, Germany. Hokkanen, H. 1989. Biological and agrotehnical control of the rape blossom beetle Meligethes aeneus (Col., Nitid.). Acta Entomologica Fennica 53: 25–29. Hokkanen, H. & Holopainen, J.K. 1986. Carabid speciesCarabid species and activity densities in biologically and conventionally managed cabbage fields. Journal of Applied Entomol- ogy 52: 209–254. Irmler, U. 2003. The spatial and temporal pattern of carabid beetles on arable fields in northen Germany (Schles-(Schles- wig-Holstein) and their value as ecological indicators. and their value as ecological indicators. Agriculture, Ecosystems and Environment 98: 141– 151. Kasparjan, D.R. (ed.). 1981. Keys to the insect of the Euro- pean part of the USSR, Volume III, Hymenoptera, Part III. Nauka: 688. (in Russian). Lancashire, P.D., Bleiholder, H., Boom, T.D. van, Langelüd- deke, P., Strauss, P., Weber, E. & Witzenberger, A. 1991. A uniform decimal code for stages of crops and weeds. Annals of Applied Biology 119: 561–601. Langmaack, M., Land, S. & Büchs, W. 2001. Effects of dif- ferent field management systems on the carabid coe- nosis in oilseed rape with special respect to ecology and nutritional status of predacious Poecilus cupreus L. (Coleoptera, Carabidae). Journal of Applied Ento- mology 125: 313–320. Lerin, J. 1987. A short bibliographical review of Trichomalus perfectus Walker, a parasite of the seed pod weevil Ceutorhynchus assimilis Payk. Bulletin IOBC wprs 10: 74–78. Lewis, W.J., Stapel, J.O., Cortesero, A.M. & Takasu, K. 1998. Understanding how parasitoids balance food and host needs: importance to biological control. Biological Control 11: 175–183. Luik, A., Tarang, T. & Voolma, K. 2001. Carabids in refor-Carabids in refor- estation areas and in the winter rape field of the forest neighbourhood. Journal of Forest Science 47: 123– 126. Meier, U. (ed.) 2001. Growth stages of mono- and dicotyle- donous plants. 2nd ed. Updated 23 Nov 2003. Cited 5 Dec 2005. Available on the Internet: http://www.bba. de/veroeff/bbch/bbcheng.pdf Metspalu, L. & Hiiesaar, K. 2002. Ristõieliste kultuuride kah- jurid. EPM�� Taimekaitse Instituut, Tartu. p. 102.EPM�� Taimekaitse Instituut, Tartu. p. 102. Murchie, A.K. & Williams, I.H. 1998a. A bibliography of the cabbage seed weevil. Bulletin IOBC wprs 21: 163–169. Murchie, A.K. & Williams, I.H. 1998b. Effect of host size on the sex of Trichomalus perfectus. Bulletin IOBC wprs 21: 177–181. Murchie, A.K., Williams, I.H. & Alford, D.V. 1997. Effects of commercial treatments to winter oilseed rape on para- sitism of Ceutorhynchus assimilis Paykull (Coleoptera: Curculionidae) by Trichomalus perfectus (Walker) (Hy- menoptera: Pteromalidae). Crop Protection 16: 199– 202. Nilsson, C. 2003. Parasitoids of pollen beetles. In: Alford, D.A. (ed.). Biocontrol of oilseed rape pests. Oxford, UK: Blackwell Science Ltd. p. 73–85. 72 A G R I C U L T U R A L   A N D   F O O D   S C I E N C E Veromann, E. et al. Oilseed rape insects in Estonia Pickett, J.A., Butt, T. M., Wallsgrove, R.M. & Williams, I.H. 1995. Minimising pesticide input in oilseed rape by ex- ploiting natural regulatory processes. In: Proceedings of the 9th International Rapeseed Congress. Cam- bridge. p. 565–571. Statistics Board 2003. Add the title of the statistics. Updated 22 July 2005. Cited 20 October 2005. Available on the Internet: http://pub.stat.ee/px-web.2001/Database/Ma- jandus/Majandus.asp. Thiele, H.-V. 1977. Carabid beetles in their enviroments. Zoophysiology and ecology 10. A study on habitat se- lection by adaptations in physiology and behaviour. Springer-Verlag, Berlin, Heidelberg, New York. 160 p. Tryapitzyn, V.A. (ed.). 1978. Keys to the insect of the Euro-1978. Keys to the insect of the Euro- pean part of the USSR, Volume III, Hymenoptera, Part II. Nauka: 758. (in Russian). Tuubel, E. & Toom, T. 1999. The influence of pesticides on arthropod predators fauna. Transactions of the Estoni- an Agricultural University 203: 180–183. Walters K.F.A., Young, J.E.B., Kromp, B. & Cox, P.D. 2003. Management of oilseed rape pests. In: Alford, D.A. (ed.). Biocontrol of oilseed rape pests. Oxford, UK: Blackwell Science Ltd. p. 43–71. Williams, I.H. 2003. Parasitoids of cabbage seed weevil. In: Alford, D.A. (ed.). Biocontrol of oilseed rape pests. Ox- ford, UK: Blackwell Science Ltd. p. 97–112. Williams, I.H. 2004. Advances in insect pest management of oilseed rape in Europe. In Horowitz, A.R. & Ishaaya, I. (eds.). Insect pest management – field and protected crops. Springer-Verlag: Heidelberg. p. 181–208.Springer-Verlag: Heidelberg. p. 181–208. Williams, I.H., Büchs, W. Hokkanen, H., Johnen, A., Klu- kowski, Z., Luik, A., Nilsson, C. & Ulber, B. 2002. MAS- TER: management strategies for European rape pests – a new EU Project. In: The BCPC Conference 18–21 November 2002. Conference Proceedings Vol. 2, Brighton, UK. p. 641–646. Williams, I.H. & Murchie, A.K. 1995. The role of parasitoids.The role of parasitoids. Agronomist, Spring 1995. p. 13–15. Vinson, S.B. 1976. Host selection by insect parasitoids. An- nual Review of Entomology 21: 109–133. Insect pests and their natural enemies on spring oilseed rape in Estonia: impact of cropping systems Introduction Material and methods Results Discussion References