Eesti Maaülikool Estonian University of Life Sciences

EESTI MAAÜLIKOOL ESTONIAN UNIVERSITY OF LIFE SCIENCES

OILSEED RAPE PESTS AND THEIR PARASITOIDS IN ESTONIA

RAPSI KAHJURID JA NENDE PARASITOIDID EESTIS

EVE VEROMANN

A Thesis for applying for the degree of Doctor of Philosophy in Entomology

Väitekiri Filosooﬁadoktori kraadi taotlemiseks entomoloogia erialal

Tartu 2007 Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences

According to verdict No 18 of April 23, 2007 the Doctoral Committee for Agricultural and Environmental Sciences of Estonian University of Life Sciences has accepted the thesis for the defence of degree of Doctor of Philosophy in Entomology.

Opponent: Dr. Samantha M. Cook Plant & Invertebrate Ecology Division Rothamsted Research Harpenden, UK

Supervisors: Prof. Anne Luik Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences Dr. Luule Metspalu Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences

Defence of the thesis: Estonian University of Life Sciences, room 1A5, Kreutzwaldi 5, Tartu on June 15, 2007, at 10.00

The publication of this thesis was funded by the Estonian University of Life Sciences © Eve Veromann, 2007

ISBN 978-9985-830-73-4 CONTENTS

LIST OF ORIGINAL PUBLICATIONS ...... 6

INTRODUCTION ...... 7 1. REVIEW OF THE LITERATURE ...... 8 1.1. Oilseed rape pests ...... 8 1.2. Parasitoids of oilseed rape pests ...... 9 2. AIMS OF THE STUDY ...... 12 3. MATERIAL AND METHODS ...... 13 3.1. Study area ...... 13 3.2. Insect sampling ...... 13 3.3. Statistical analysis ...... 14 4. RESULTS ...... 15 4.1. Species composition and phenology of oilseed rape pests ...... 15 4.2. Species composition and phenology of parasitoids of oilseed rape pests ...... 16 4.3. Impact of cropping system and insecticide use on the abundance of oilseed rape pests and their parasitoids ...... 18 5. DISCUSSION ...... 20 5.1. Comparison of pest species in winter and spring oilseed rape ...... 20 5.2. Comparison of parasitoids of oilseed rape pests in winter and spring oilseed rape ...... 21 5.3. Comparison of impact of cropping systems and insecticide use on the abundance of oilseed rape pests and their parasitoids ...... 23 6. CONCLUSIONS ...... 25 REFERENCES ...... 27 SUMMARY IN ESTONIAN ...... 32 ACKNOWLEDGEMENTS ...... 35

ORIGINAL PUBLICATIONS ...... 37 CURRICULUM VITAE ...... 78 LIST OF PUBLICATIONS ...... 82 LIST OF ORIGINAL PUBLICATIONS

This thesis is a summary of the following papers, which are referred to by Roman numerals in the text. The papers are reproduced by kind per- mission of the publishers of the following journals: Entomologica Fen- nica (I), Agricultural and Food Science (II), International Journal of Pest Management (IV)

I Veromann, E., Luik, E., Metspalu, L. & Williams, I. 2006. Key pests and their parasitoids on spring and winter oilseed rape in Es- tonia. Entomologica Fennica 17, 400–404.

II Veromann, E., Tarang, T., Kevväi, R., Luik, A. & Williams, I.H. 2006. Insect pest and their natural enemies on spring oilseed rape in Estonia: impact of cropping systems. Agricultural and Food Sci- ence, 15, 61–72.

III Veromann, E., Luik, A. & Kevväi, R. 2006. Oilseed rape pests and their parasitoids in Estonia. Bulletin IOBC/wprs, Integrated Con- trol in Oilseed Crops, 29 (7), 165–172.

IV Veromann, E., Kevväi, R., Luik, A. & Williams, I.H. 2007. Do cropping system and insecticide use in spring oilseed rape affect the abundance of pollen beetles (Meligethes aeneus Fab.) on the crop? – International Journal of Pest Management, in press.

6 INTRODUCTION

Oilseed rape (Brassica napus L.) is one of the most important oilseed plants cultivated in temperate regions. The expansion of the growing area of rape in Europe has resulted in an increase in the number of pests (Büchi, 1996; Cook et al., 1999; Hokkanen, 2000). In Estonia, the area sown to the crop has increased greatly during the last ﬁfteen years, with 50,400 hectares grown in 2004 (Statistics Estonia, 2006). The management of pests on the European oilseed rape crop still relies heavily on chemical pesticides, most often applied routinely and prophylactically, without regard to pest incidence, at best according to threshold values of the pest population (Williams, 2004). This leads to the over-use of chemical pesticides, which reduces the economic competitiveness of the crop, brings on the development of resistance to pesticides and also threatens biological diversity. Pesticides also kill natural agents of biological control that represent a resource with a great potential beneﬁt to farmers and consumers (Alford et al., 1995; Williams & Murchie, 1995; Walters et al., 2003). By killing the natural enemies of pests, pesticide use has to be increased further to achieve pest control (Pickett et al., 1995; Murchie et al., 1997).

Recent advances in insect management of the pests of oilseed rape have emphasised the important role of natural enemies within integrated pest management systems for the crop (Williams, 2004). To develop economically-viable and environmentally-acceptable crop management strategies for oilseed rape to maximise the biocontrol of key pests and minimise chemical inputs requires a much better understanding of pest and parasitoid taxonomy and biology throughout Europe. In Estonia, cropping with spring rape is still prevalent but growing of winter rape is also increasing. As Estonia is at the northernmost latitude for growing winter rape, winter survival of the crop is always questionable. The pests of oilseed rape and their natural enemies have been little studied in Esto- nia. The present study was focused on the identiﬁcation of key pests and their parasitoids and determination of factors affecting their occurrence on both winter and spring oilseed rape.

7 1. REVIEW OF THE LITERATURE

1.1. Oilseed rape pests

The major pests of oilseed rape in Europe are the pollen beetle, Meligethes aeneus (Fabricius) (Coleoptera, Nitidulidae), the cabbage seed weevil, Ceutorhynchus assimilis (Paykull), the cabbage stem weevil, C. pallidactylus (Marsham), the rape stem weevil, C. napi Gyllenhal (Coleoptera, Curculionidae), the cabbage stem ﬂea beetle, Psylliodes chrysocephala (Linnaeus) (Coleoptera, Chrysomelidae) and the brassica pod midge, Dasineura brassicae (Winnertz) (Diptera, Cecidomyiidae) (Alford et al., 2003; Williams, 2004). Flea beetles (Phyllotreta spp., Coleoptera, Chry- somelidae) are also important, particularly on spring oilseed rape, the most frequent ones being P. nemorum (Linnaeus), P. atra (Fabricius), P. undulata (Kutschera) and P. nigripes (Fabricius). Some of these pests occur virtually everywhere where rape is grown, whereas others have a more limited distribution. None of these pests are speciﬁc to the oilseed rape crop, although all are crucifer-specialists. Many other crucifer-specialist insects also occur on the crop, without attaining pest status (Alford et al., 2003).

In Estonia, knowledge of the pests of oilseed rape is fragmentary and largely conﬁned to the description of species. There was great shortage of literature about oilseed rape pest biology, abundance and the damage they cause. First data of oilseed rape pests and their control with pesticides date from Lõiveke (1991) and Kaarli (2000). More detailed descriptions of pests of brassicaceous crops are given by Metspalu & Hiie- saar (2002).

With participating in the EU-funded project MASTER: MAnagement STrategies for European Rape pests, the Estonian Science Foundation Grant in 2002 and the project of Estonian Ministry of Agriculture in 2004, systematic studies of oilseed rape pests and investigations of factors inﬂuencing their presence and abundance were started in the De- partment of Plant Protection of the Estonian University of Life Sciences. The aims of the MASTER project were to develop economically-viable and environmentally-acceptable crop management strategies for winter oilseed rape which maximise the biological control of key pests and min-

8 imise chemical inputs (Williams et al., 2002). Chemical control of pests of oilseed rape still prevails. Although insecticides can effectively control the pests, there is an urgent need to develop alternative strategies for managing them (Williams, 2004). Several studies already indicate that M. aeneus has developed resistance to pyrethroids in France, Denmark and Sweden (Hansen, 2003; Nilsson & Ahman, 2006). The need to reduce dependence of chemical inputs in pest management has lead to investigation of the possibilities for developing sustainable crop management. The preservation and improvement of soil fertility and of the crop environment are vital elements of sustainable farming (Walters et al., 2003). Integrated pest management considers the whole farm as a unit, including the non-farmed land, to enhance biodiversity and landscape features. Minimal cultivation techniques tend to be preferred in integrated crop management, because of reduction of energy input, miner- alization and leaching of nitrogen, improvement of the physical qualities of the soil; reduction of soil erosion, and the increase in populations of beneﬁcial organisms (Walters et al., 2003). Therefore, it is necessary to explore possible agro-technological ways to reduce chemical inputs and optimise biological control also in Estonia.

1.2. Parasitoids of oilseed rape pests

Herbivorous pests are commonly subject to varying levels of attack by natural enemies, many of which help to limit pest populations. Most of the important insect pests of oilseed rape in Europe are attacked by hymenopterous parasitoids, notably braconid wasps (Braconidae, Hy- menoptera), ichneumonid wasps (Ichneumonidae), and chalcid wasps (Pteromalidae) that attack the larvae (Alford, 2000), and these are being exploited for bio-control in integrated pest management strategies for the European rape crop (Williams et al., 2003).

Meligethes aeneus, is known to be attacked by nine species of parasitoid: Tersilochus heterocerus Thomson, Phradis morionellus (Holmgren), P. interstitialis (Thomson), Aneuclis incidens (Thomson) (all Ichneumo- nidae), Diospilus capito (Nees), Blacus nigricornis Haeselbarth, Eubazus sigalphoides (Marshall) (Braconidae), Cerchysiella planiscutellum (Mercet) (Encyrtidae) and Brachyserphus parvulus (Nees) (Proctotrupidae) (Nils- son & Andreasson, 1987; Nilsson, 2003); the most effective of these are P. morionellus and D. capito. For example, in Switzerland, over 60% of

9 M. aeneus larvae have been reported attacked by these parasitoids (Bil- lqvist & Ekbom, 2001a, b).

Ceutorhynchus assimilis is attacked by parasitoids of all stages of its life cycle, although most of the parasitism is directed towards the larval stage (Murchie & Williams, 1998a). More than 30 species of hymenopterous parasitoids have been reported to attack C. assimilis in Europe (Alford, 2000; Williams, 2003) and can provide natural control of this pest. The most commonly cited parasitoids are ectoparasitoids of the larval stage, namely, Trichomalus perfectus, Mesopolobus morys (Walker), and Stenoma- lina muscarum (Linnaeus) (Pteromalidae). Of these, T. perfectus is widely distributed and particularly important (Lerin, 1987; Murchie & Wil- liams, 1998a,b; Murchie et al., 1999; Williams, 2003). In addition to killing larvae through direct parasitism, it further reduces damage to infested pods by preventing host larvae from eating their full complement of seeds (Murchie & Williams, 1998b).

Two species of the subfamily Tersilochinae (Ichnemonidae), T. fulvipes (Gravenhurst) and T. moderatus Linnaeus parasitize the larvae of C. napi, where the level of the parasitism may be as high as 95% (Alford, 2000).

The most important parasitoids of C. pallidactylus are Tersilochus obscurator Aubert, T. tripartitus Brischke, T. exilis Holmgren and Stibeutes curvispina (Thomson) (Ulber, 2000; Barari et al., 2004).

Psylliodes chrysocephala (L.) is attacked by parasitoids its larval and adult stages also. The larval parasitoids are T. tripartitus, T. microgaster (Szép- ligeti), Aneuclis melanarius (Holmgren), Diospilus morosus Reinhardt (Ulber & Willams, 2003; Barari et al., 2004). Aneuclis melanarius and D. morosus are multivoltine larval endoparasitoids of several coleopteran species.

Diospilus morosus is most common parasitoid of Phyllotreta nemorum L. (large striped ﬂea beetle) also (Ulber & Willams, 2003). In total, 28 species of parasitoids attack D. brassicae, but the most widespread and frequently reported parasitoid in Europe appears to be Platygaster spp. (Hymenoptera: Platygastridae) (Williams, 2003). Omphale clypealis (Thomson) (Eulophidae) is the second most commonly cited larval endoparasitoid of D. brassicae (Williams, 2003). In Estonia, the ﬁrst data about the parasitoids of oilseed rape pests is published in my master the-

10 sis (Veromann, 2003), but as the subject is a difﬁcult one, there is still a lot to do. It is very important to ﬁnd out which species of hymenopteran parasitoids attack oilseed rape pests in Estonia, whether they can control the pest population and how their activities as natural control agents can be enhanced.

Naturally-occurring biocontrol agents are widely distributed and often common on oilseed rape crops, and hence are a valuable natural resource (Walters et al., 2003). It may be possible to enhance conservation biological control by modifying some current crop husbandry practices to promote the survival of natural populations of parasitoids. As part of the MASTER project, the effect of ploughing versus non-inversion tillage on the over-winter survival of key parasitoids of the target pests of winter oilseed rape was investigated (Nilsson et al., 2006b). There is evidence that minimal (non-inversion) tillage throughout the rotation promotes predators as well as parasitoids that overwinter in the soil (Nilsson, 1985; Hokkanen, 1989; Walters et al., 2003). Also timing of applying insecticides has crucial importance for conserving parasitoids. Avoidance of flowering and post-flowering treatments when parasitoids are most active conserves their natural populations (Williams, 2004, 2006). In addition, spatial targeting of insecticides could help decrease parasitoid mortality (Ferguson et al., 2003). Hypothetically, if only a part of the pest population were killed by insecticide treatment without damaging the parasitoid population, the parasitoid to host ratio would be increased, enhancing biological control of the pest. To find out how to conserve and enhance the presence and abundance of natural enemies of pests in our agricultural landscapes is a key question in environmentally sustainable production of crop. However, enhancing biological control of oilseed rape pests is a very complicated task, involving many interacting factors such as plant species, variety, structure, soil tillage, parasitoids, predators, pesticide use etc. (Nilsson et al., 2006a). New information on the pest-parasitoid community in the crop ecosystem and the agricultural technologies affecting it is essential for the development of environmentally-sustainable crop management.

11 2. AIMS OF THE STUDY

In Estonia, knowledge of the pests of oilseed rape and their hymenopterous parasitoids is fragmentary and largely conﬁned to the description of species. To develop economically-viable and ecologically-sustainable rape cultivation technologies in Estonia, the most important rape pests and their parasitoids present must be identiﬁed. The aims of this study were:

1. To identify key pests and their parasitoids on winter and spring oilseed rape in Estonia and to compare the species biology on winter and spring crops. (I, II, III).

2. To compare the impact of reduced input (no plough, direct drilling, no pesticides) and conventional (plough, standard application of pesticides) cropping systems on the occurrence of pests and their hymenopteran parasitoids on winter and spring oilseed rape (II, III, IV).

12 3. MATERIAL AND METHODS

3.1. Study area

A study with an organically-grown winter oilseed rape crop (WOSR) was carried out on Puki farm, Tartu County in 2002 (I). From 2003 to 2005, the study with winter and spring oilseed rape (SOSR) was carried out on Pilsu Farm, Tartu County (I, II, III, IV). Pilsu Farm was chosen because it is one of the few farms with experience of growing both the winter as well as spring oilseed rape for more than 15 years. In all probability, there is developed a local population of oilseed rape pests and their parasitoids. Therefore, this farm was selected as a model-farm and the results were generalised to Estonia. Winter and spring oilseed rape were grown with a reduced input, referred to here as minimised (MIN), and standard (STN) cropping systems. The study site included two adjacent, approximately rectangular, 2 ha (I, II, IV) or 1 ha fields (two replicates for both crops) (III). In the STN system ploughing and pesticides were used. The herbicides were applied before drilling and at the two-leaf growth stage (BBCH-stage 12 of Meier (2001), see also Lancashire et al., 1991). The fungicide was applied at BBCH 50−51. The insecticides were used at green bud stage (BBCH 51), at full flowering of main raceme (BBCH 65−66) and at the end of flowering of the main raceme of oilseed rape plants (BBCH 67−69) (II, III, IV). In the MIN system, direct drilling replaced ploughing (except in SOSR in 2005, IV) and no pesticides were applied.

3.2. Insect sampling

Insects were sampled using yellow water traps (210 x 310 x 90 mm deep). Yellow water traps have been used extensively to sample pests and their parasitoids in oilseed rape (Williams et al., 2003). Yellow is the most effective colour for trapping them. Traps placed at the top of the canopy are particularly effective for sampling insects that fly within the upper canopy e.g. the inflorescence pest M. aeneus and C. assimilis and their parasitoids, but not as effective for stem-mining pests and their parasitoids, which fly lower in the canopy. Traps were put out after sowing (II), at the beginning of flowering (BBCH 60–62) (I, III, IV), and

13 emptied weekly until just before harvest (BBCH 83). They were positioned at the top of the crop canopy and raised weekly to keep pace with crop growth. Insect samples were sorted in the laboratory, phytophagous crucifer-specialist insects and all hymenopterous parasitoids were separated and stored in 70% ethanol at -18 °C, for later identiﬁcation and counting of key species.

For estimation of parasitisation levels (III), M. aeneus larvae were collected from oilseed rape ﬂowers from 25 randomly chosen plants on each plot. Larvae were dissected in the laboratory for estimation of presence of parasitoid larvae. For the establishment of damage and parasitisation assessments of C. assimilis, 25 plants were selected from each plot and all their pods were collected and incubated in emergence traps in laboratory conditions. Emerging parasitoids and larvae were counted and the percentage of damaged pods calculated.

3.3. Statistical analysis

Statistical analysis was carried out using the SAS GENMOD procedure. Comparisons of the numbers of pests, parasitoids and generations of pests were made using type 3 empirical standard errors analysis and the Poisson distribution and the log link function (II, III, IV). The numbers of pests caught each week were also analysed separately (II). The weekly target of pests and parasitoids were analysed applying the Poisson distribution and the log link function (II, III, IV). For the repeated measures the generalized estimation equation analysis was used. The scale parameter was estimated by Pearson’s chi-square divided by the degrees of freedom if the model was overdispersed (III, IV).

14 4. RESULTS

4.1. Species composition and phenology of oilseed rape pests

During the study, 334 samples of WOSR and 408 samples of SOSR with a total of 25,945 specimens of crucifer-specialist insect pests from nine taxa were collected from the water traps (Fig. 1) (I, II, III, IV). A more abundant crucifer-specialist community was found in the spring oilseed rape (19,296 specimens) than in the winter oilseed rape (6,649 specimens).

Meligethes aeneus was the most numerous crucifer-specialist in both crops; however the numbers in the SOSR were 5.9 times greater than in the WOSR. The second most abundant pest was C. assimilis, but in contrast to M. aeneus, their number was 6.9 times greater in winter than in spring rape. In addition, M. viridescens Sturm, C. pallidactylus, C. rapae (Gyllenhal), C. typhae (Herbst) (synonym C. ﬂoralis Paykull (Alonso- Zagazaga, 2004) is used in publication I), C. pleurostigma (Marsham), C. sulcicollis (Paykull) and ﬂea beetles (Phyllotreta spp.) were also captured (I, II, III).

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Figure 1. The species composition and the total number of crucifer-specialist insects caught in yellow water traps in winter (WOSR) and spring (SOSR) oilseed rape on Puki and Pilsu Farm, Tartu County, Estonia, in 2002−2005 (I, II, III, IV).

15 Meligethes aeneus started to colonise winter rape from the full flowering stage of plants (BBCH 63−66) and its population peaked at the same time. The second peak occurred during pod development (BBCH 70−72) (I, III). This second peak occurred simultaneously with the beginning of colonisation of spring rape (II, III). In spring rape, the first pollen beetles were caught at the two leaf-stage (BBCH 12) (I, II). Their numbers increased steadily and M. aeneus had its first population peak when plants were at the green bud stage (BBCH 50) (I, II, III). Then their numbers decreased again with a new increase after three weeks during pod maturation (BBCH 79–80) (I, II, III).

The first C. assimilis were found at the beginning of full flowering of winter oilseed rape (BBCH 63) and their abundance increased at pod development stage (BBCH 72) (I, III). Their number was the greatest during pod maturation (BBCH 79–80) (I, III). In spring rape, their abundance was low throughout the study period. The first seed weevils were found at the four-leaf stage (BBCH 14) (II). There were two population peaks, the first during flowering (BBCH 59–65) and the second during pod maturation (BBCH 79–80) (I, II, III).

4.2. Species composition and phenology of parasitoids of oilseed rape pests

During the study, hymenopteran parasitoids from six superfamilies and 18 families were captured in the water traps. Amongst them were four parasitoids of M. aeneus: D. capito, P. morionellus, P. interstitialis and T. heterocerus and three parasitoids of C. assimilis: S. gracilis, M. morys and T. perfectus. In total, the numbers of parasitoids of M. aeneus were 10.3 times greater than those of C. assimilis. The number of parasitoids in spring rape was 1.4 times greater than in winter oilseed rape (Fig. 2). In the ﬁrst study year in 2002, only four specimens of key parasitoids were caught from winter oilseed rape (I). Next year in 2003, Phradis morionellus was the dominant species in spring rape (I). In 2005, Diospilus capito was the most abundant parasitoid in both crops. However, the numbers in the spring crop were 1.4 times greater than those in the winter crop (III). Phradis morionellus was the second most abundant; it was 1.9 times smaller than D. capito but 1.7 times greater than P. interstitialis (III). Similarly to D. capito but in contrast to P. interstitialis, P. morionellus was more numerous in the spring crop (III). Only a single specimen of T. heterocerus was

16 ��

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Figure 2. The species composition and the total number of key parasitoids of oilseed rape pests caught in yellow water traps in winter (WOSR) and spring (SOSR) oilseed rape on Puki and Pilsu Farm, Tartu County, Estonia, in 2002–2005 (I, II, III).

found in SOSR in 2003 (I). A total of 24 specimens of the C. assimilis larval ectoparasitoids: M. morys, S. gracilis, T. perfectus, in the winter oilseed rape ﬁeld and 32 specimens in the spring oilseed rape ﬁeld were found. A total of nine specimens of S. gracilis, 17 specimens of M. morys and 30 specimens of T. perfectus were found (I, II, III).

In the winter oilseed crop, the number of parasitoids started to increase at the pod development stage (BBCH 70–72) and peaked at the end of pod development (BBCH 78) (III). In the spring oilseed rape ﬁeld, the number of parasitoids increased as the rape started to ﬂower (BBCH 59– 60) and were most numerous during pod ripening (BBCH 79–80)(I, III). During the population peaks of the parasitoids, the dominant species in both crops was D. capito (III).

Meligethes aeneus and C. assimilis larval infestation by parasitoids was estimated in larvae collected from both crops. The larvae of D. capito and Phradis spp. were found from larvae of M. aeneus. The ectoparasitoids of C. assimilis, T. perfectus, M. morys and S. gracilis were reared from oilseed rape pods. Larval parasitisation rate of C. assimilis reached 32% and of M. aeneus 7% (III).

17 4.3. Impact of cropping system and insecticide use on the abundance of oilseed rape pests and their parasitoids

In winter oilseed rape, the abundance of M. aeneus and C. assimilis was higher in the MIN than in the STN field in 2005 (III). Because of the late spring in 2005, M. aeneus could oviposit in winter oilseed rape also. Dissection of larvae of M. aeneus (collected from flowers at the end of flowering (BBCH 67–69) showed that the parasition rate of larvae was greater in the MIN than in the STN field (III). Treatment with insecticides decreased C. assimilis damage. In the STN field, 4.5% of pods and in the MIN field, 14.4% of the pods were damaged, but larval parasitisation level was higher in the STN than in the MIN field. As with the pests, the abundance of their parasitoids was significantly greater in the MIN than in the STN field (III).

In spring oilseed rape population of M. aeneus showed a general increase in size from 2003–2005 (Fig. 3) (IV). The old generation (previously overwintered) population was smallest in the MIN field in 2003. In each year, the old population was greater in the STN than in the MIN, but the difference was statistically significant only in 2003. In both MIN and STN fields, the old generation was greatest in 2005, and differed significantly that in all other years (IV, table 2, p. 77). Similarly to the

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Figure 3. Mean abundance (± SD) of old and new generation of M. aeneus per trap on Pilsu Farm, Tartu County, 2003–2005.

18 old generation, the size of the new generation to emerge from soil was smallest in the MIN field in 2003. The new generation population size was greater in STN than in MIN fields, with differences significant in 2003 and in 2005 (IV, table 2, p. 77). The new generation population size was significantly greater in the STN field of 2005 than in all other years (IV).

In spring rape, C. assimilis abundance was greater in the MIN than in the STN field (III), 0.6% and 3.7% of pods were damaged, respectively. No parasitoids were found in larvae from the STN field, but larval parasitisation reached 32% in the MIN field. Numbers of key parasitoids of oilseed rape pests were greater in the MIN than in the STN field (III).

19 5. DISCUSSION

5.1. Comparison of pest species in winter and spring oilseed rape

The species spectrum of the oligophagous pests of winter and spring rape was similar (Fig. 1), but their ﬂight phenologies differed. During the study, the three major European pests: M. aeneus, C. assimilis and C. pallidactylus were collected. The latter was not numerous – only a few specimens were found in winter oilseed rape and it was very rare in spring oilseed rape (I, II, III). Meligethes aeneus was by far the most numerous and the only one to reach pest status (Fig. 1). Meligethes aeneus emerges from hibernation sites in the middle of May in Estonia. In spring rape it accounted for 96.1% of the crucifer-specialist specimens caught from the crop, six fold more than on winter oilseed rape. By contrast, the numbers of C. assimilis caught on winter rape were seven fold those on spring rape. They emerged in spring and used the winter rape for maturation feeding. Meligethes viridescens and C. typhae were relatively abundant in WOSR in 2002 (see also Tarang et al., 2004), but only a few were caught in 2005. Meligethes viridescens requires higher temperatures for oviposition and development than M. aeneus (Alford et al., 2003). In addition, this species prefers to reproduce in wild cruciferous plants (Billqvist & Ekbom 2001a, 2001b). Notwithstanding, C. typhae was unexpectedly abundant in 2002. It does not have pest status in oilseed rape; according to the literature, this species is an early spring species, which passes through its development cycle on spring weeds (I). The abundance of other captured crucifer-specialists was low in the both crops (I, II, III).

Although the numbers of M. aeneus in winter oilseed rape were large, they arrived when the plants were mostly past the bud stage suitable for oviposition. Hiiesaar et al. (2003), Tarang et al. (2004) and Veromann et al. (2004, 2005) have shown that M. aeneus does not damage winter oilseed plants in Estonia; it uses winter rape for maturation feeding and moves to the spring rape for oviposition. By contrast, in spring rape their ﬁrst population peak coincided with the green bud stage, when the crop is most vulnerable to damage. Green bud stage is the most suitable period for egg laying by M. aeneus (Alford et al., 2003). The second peak during pod maturation indicated emergence of the new generation from the soil. The population of M. aeneus was phenologically better synchro-

20 nised with spring oilseed rape, where numerous individuals of the new generation developed.

Phenological synchrony of C. assimilis was better with the growth of the winter crop than with that of the spring crop. Their abundance in WOSR increased at pod development stage, which is suitable time for egg laying (I, III). Second peak during pod maturation stage is probably related to a new generation (III). In spring rape, both population peaks of C. assimilis were unsuitable for oviposition. Probably by the time spring oilseed rape had reached the young pods growth stage suitable for egg laying by this weevil, it had already laid eggs on other suitable cruciferous plants.

There are several reasons for the differences in incidence of pests on spring and winter rape. One important reason is that the phenological development of the crop may be asynchronous with the development of the pests. This can be influenced greatly by weather conditions of the year. For example, in a dry and warm spring, winter rape may complete flowering too early to provide flower buds for M. aeneus oviposition. Similarly, for C. assimilis, winter rape may be past its optimal growth stage for oviposition by the time the pest arrives on the crop. Further, hibernating insects may be killed by severe winter conditions so that emerging populations may be too small to damage the crop. As in Fin- land (Hokkanen 1993, 2000), overwintering mortality could be a main factor determining population size.

5.2. Comparison of parasitoids of oilseed rape pests in winter and spring oilseed rape

Parasitoid occurrence of both key pests was established in both crops. Four parasitoids of M. aeneus: D. capito, P. morionellus, P. interstitialis and T. heterocerus and three parasitoids of C. assimilis: S. gracilis, M. morys and T. perfectus were captured. All were recorded for the ﬁrst time from Estonia. These parasitoid species have been found over most of Eu- rope, from southern Sweden to France (Nilsson, 2003) and D. capito and P. morionellus parasitoids of M. aeneus have also been found in Finland (Hokkanen, 1989). The distribution and abundance of different species depends on factors such as the local climate, the crops grown during previous years and the cultivation techniques used (Nilsson, 2003).

21 Diospilus capito and P. morionellus were the two dominant species throughout the study period, on both crops. Diospilus capito is multivoltine with two or three generations in northern Europe (Billquist & Ekbom, 2001b; Nilsson, 2003). As the population of multivoltine parasitoids in winter rape has been reported as very low (Nilsson, 2003), the high numbers of D. capito in winter rape in our study was surprising. The other important M. aeneus parasitoid in Northern Europe, P. morionellus was more numerous in the spring crop. By contrast to our results, in Finland P. morionellus is the dominant species and its parasitism rate may reach until 70% (Hokkanen, 2006). Likewise in Sweden, P. morionellus is recognised as an abundant and effective regulator of its host (Billqvist & Ekbom, 2001a). Phradis interstitialis is absent from Finland, but was found in both winter and spring crops quite evenly.

The abundance of C. assimilis parasitoids caught from the winter and spring rape was similar and relatively low. Trichomalus perfectus was the most abundant parasitoid amongst them. Trichomalus perfectus is a univoltine ectoparasitoid whose abundance peaks 2–4 weeks after migration of C. assimilis into the crop. New-generation parasitoids mate on emergence and leave the crop shortly before harvest. Only females overwinter, possibly in evergreen foliage (Williams, 2003).

The diversity and abundance of parasitoids, like that of their hosts was greater on spring than on winter rape. Veromann et al. (2006a) showed that, in 2003–2005 populations, all parasitoids were signiﬁcantly greater on spring oilseed rape than on winter crops. Also, the population of parasitoids of M. aeneus was greater than the population of parasitoids of C. assimilis (Veromann et al., 2006a). Therefore, parasitoid phenology was synchronised with that of their hosts. Peak abundance of the most numerous parasitoid, D. capito, coincided with peak abundance of M. aeneus in both ﬁelds, indicating, that they probably emerged from host larvae in the oilseed rape.

Incidence of insects in oilseed rape is dependent on several factors such as plant architecture, presence of ﬂowering weeds, crop rotations, landscape structure etc. (Walters et al., 2003). Weeds can exert direct stress on crops (by competing for sunlight, moisture etc.) or affect indirectly through enhancing the presentation of pests natural enemies (Altieri & Nicholls, 2004) (I, II, III).

22 5.3. Comparison of impact of cropping systems and insecticide use on the abundance of oilseed rape pests and their parasitoids

In winter oilseed rape, treatment with insecticides decreased the abundance of M. aeneus and C. assimilis but also had a detrimental impact on their parasitoids, as the abundance of parasitoids and the parasition rate of larvae was greater in the MIN than in the STN ﬁeld (III).

In spring rape, despite the application of insecticide to the STN field, the old generation of M. aeneus was more abundant in the STN than in the MIN fields (Fig. 3). Overwintered M. aeneus adults colonized both cropping system in similar numbers, but treatment of the STN fields with insecticide reduced the numbers of M. aeneus at the vulnerable green bud stage of the crop. As a consequence, the plants in the STN field were able to produce noticeably more flowers than those in the MIN fields. STN fields treated with insecticide consequently offered more buds and flowers suitable for feeding and egg laying than the MIN fields not treated with insecticide, and, for that reason, were more attractive to the old generation of M. aeneus than the MIN fields. The new generation M. aeneus showed a strong linear increase in size over the three years, being always greater in fields with insecticide treatment. According to Hokkanen (2000), insecticide treatment at or above the threshold level will not significantly reduce the size of the new generation, because the maximum number of new generation adults emerge from the soil from much lower old generation beetle densities. Spraying only helps to protect the crop yield of one season. Our study showed that treatment of the old generation with insecticides increased the size of the new generation as the number of emerged beetles was always greater in the STN than in the MIN fields (IV). What is more, because the size of the population of M. aeneus in the STN fields was always greater than in the MIN fields, it is possible that the pest may have developed resistance to pyrethroids. Abundance of C. assimilis was very low in both cropping systems in the spring rape, but unlike M. aeneus, their abundance was greater in the MIN field than in the STN field (II, III). The level of parasitism of C. assimilis larvae was also dependent on insecticide application as no parasitoids were found from the treated field (III, IV). The number of parasitoids was greater in the MIN than in the STN field, except at full flower of plants in 2003 when their number was greater in the STN field. In this case, they probably were attracted by the greater abundance of flowers; adult parasitoids are exclusively dependent on floral and ex-

23 traﬂoral nectar, honeydew and pollen for food (Lewis et al., 1998). Dur- ing pod ripening (BBCH 79–80), the further increase in the number of parasitoids in the MIN ﬁeld probably indicated the emergence of new generations of some hymenopteran parasitoid species (II, III).

Application of insecticide may thus not only result in more buds and flowers for feeding and egg-laying by M. aeneus and C. assimilis but probably also kills their natural enemies, which have potential to decrease the size of the new generation of these pests. Insecticides are known to kill both parasitoids (Hokkanen et al., 1988; Hokkanen, 1989; Hokkanen, 2006; Nilsson, 2003; Williams, 2004) and predators (Büchs, 2003; Büchs et al., 2006; Hokkanen & Holopainen, 1986; Veromann et al., 2006b; Williams, 2004) in oilseed rape field. Our study (II, III) and Luik et al. (2006) showed that the population size, number and species diversity of hymenopteran parasitoids and predators was greater in fields with MIN than in those with STN cropping systems. Further, in the STN system, ploughing probably reduced parasitoid survival and diminished predator species diversity and abundance, whereas MIN cultivation was less destructive as found by Büchs 2003, Nilsson 1985, Nilsson et al. 2006b and Williams 2004. The cropping system appeared to have influenced rape plant architecture, enabling plants of the STN field to produce more flowers than those in the MIN field, which in turn resulted in greater infestation by M. aeneus in the former.

24 CONCLUSIONS

1. During the study, crucifer-specialist insect pests from nine taxa were collected in winter and spring oilseed rape ﬁelds. Amongst them were three major European pests of oilseed rape: Meligethes aeneus, Ceutorhynchus assimilis and C. pallidactylus. Two of them, Meligethes aeneus and Ceutorhynchus assimilis, were most abundant and could inﬂuence oilseed rape production in Estonia (I, II, III).

2. Other pests of importance in other European rape-growing areas do not yet appear to have reached pest status in Estonia, where the crop is relatively new, although many potential pests are present. They may be surviving on wild relatives of Brassica crops and may adapt in time to synchronise their life cycles with that of oilseed rape (I, II, III).

3. In 2003–2005, winter oilseed rape had no serious pest problem. The abundance of M. aeneus was low and their phenology was poorly synchronized with crop. The population of C. assimilis was phenologically better synchronised with winter rape where their reproduction mainly takes place. Although their numbers were too low to cause yield loss (I, III). Other studies have also shown that, in Estonia, winter rape is less vulnerable than spring rape, partly due to earlier ﬂowering, partly due to a longer growth season to compensate for attack (Tarang et al., 2004; Veromann et al., 2004) (I, II, III).

4. On spring oilseed rape in 2003–2005, M. aeneus was the only crucifer-specialist who had reached real pest status. The numbers of M. aeneus in spring oilseed rape were large and their population showed linear increase in size over the years. By contrast, the abundance of C. assimilis was low as well as their oviposition activity because of asynchronous phenological development between the crop and weevil. By the time spring oilseed rape had reached the young pods growth stage suitable for egg-laying by C. assimilis, it had already laid eggs on other suitable cruciferous plants.

25 5. The parasitoids of key pest species present in winter and spring oilseed rape were established. Meligethes aeneus larval parasitoids: Diospilus capito, Tersilochus interstitialis, Phradis morionellus and P. interstitialis and C. assimilis larval ectoparasitoids: Trichomalus perfectus, Mesopolobus morys and Stenomalina gracilis were found. All were recorded for the ﬁrst time from Estonia. The numbers of parasitoids of M. aeneus was greater than parasitoids of C. assimilis. Therefore, parasitoids phenology was synchronised with that of their hosts. The most numerous parasitoid on both crop was D. capito. The numbers of parasitoids were low because the history of oilseed cropping in Estonia is not long. Probably the parasitoids need more time to build up their populations. Although their greater abundance and parasitisation rate in the minimised cropping system ﬁeld suggests potential to encourage them with more environmentally-friendly crop management. (I, II, III).

6. Treatment with insecticides on winter oilseed rape decreased the abundance of M. aeneus and C. assimilis but it had also detrimental impact on their parasitoids (III). In spring rape, the new generation M. aeneus showed a strong linear increase in size over the three years, being always greater in ﬁelds with insecticide treatment (IV).

7. Reduced input cropping system promoted the presence of natural enemies of M. aeneus and C. assimilis and standard cropping system promotes the increase of the population M. aeneus (III, IV).

26 REFERENCES

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31 SUMMARY IN ESTONIAN

RAPSI KAHJURID JA NENDE PARASITOIDID EESTIS

Raps (Brassica napus L.) on üks tähtsamaid parasvöötmes kasvatatavaid kultuurtaimi. Kuivõrd rapsi kasvupinnad on eriti viimasel aastakümnel ka Eestis kordades suurenenud, on ristõieliste kahjurite arvukuse kas- vuks loodud soodsad tingimused, sest suured monokultuursed põllud pakuvad piiramatult toitu ning paljunemisvõimalusi taimekahjuritele ning kahjurite looduslikud vaenlased ei pääse mõjule. Aastaid on rapsi- kahjureid tõrjutud püretroididega, enamasti rutiinselt ja profülaktiliselt, kahjurite kohalolekut ja ohtrust kontrollimata. Selle tagajärjeks on pestit- siidide liigne ja vähemõtestatud kasutamine, mürgi suhtes resistentsete kahjurite kujunemine, saagi majandusliku konkurentsivõime vähene- mine ning põldude bioloogilise mitmekesisuse kahanemine. Pestitsiidid tapavad koos kahjuritega ka nende looduslikud vaenlased, kes võiksid tuua põllumehele suurt kasu, hoides kahjurite arvukuse loodusliku kont- rolli all.

EMÜ PKI taimekaitse osakonnas algas 2002. aastal rapsikahjurite ja nende parasitoidide ning nende arvukust mõjutavate tegurite süstemaati- line uurimine eesmärgiga arendada majanduslikult tasuvaid ja ökoloogi- liselt säästvaid rapsikasvatuse tehnoloogiaid. Sellest lähtuvalt oli esma- tähtis määrata kindlaks nii tali- kui suvirapsi peamised kahjurid ja nendega seotud looduslikud vaenlased.

Käesoleva töö raames selgitati tali- ja suvirapsi kahjurite ja nende parasitoidide liigiline koosseis, arvukus, selle dünaamika ning neid mõjutavad tegurid (I, II, III). Võrreldi rapsi kahjurite ja nende kiletiivaliste parasitoidide esinemist erineva kasvatustehnoloogiaga põldudel, kusjuures vaatluse all olid tavaviljelusega (STN – künd, mullaharimine, insektitsiidide kasutamine vastavalt tehnoloogilisele skeemile) ja minimeeritud viljelusega (MIN – kõrdekülv, insktitsiidide ei kasutatud) suvi- ja talirapsi põllud (II, III, IV).

Putukate püüdmiseks kasutati vesipüüniseid. Tali- ja suvirapsilt kogutud ristõielistele taimedele spetsialiseerunud putukad kuulusid üheksasse tak- sonisse (I, II, III). Tulemustest selgus, et kahjurite liigispekter ei sõltunud

32 rapsi erinevatest vormidest, see oli nii tali- kui suvirapsil enam-vähem sar- nane. Oluline erinevus ilmnes aga arvukuses – suvirapsil oli ristõielistele spetsialiseerunud kahjureid märgatavalt rohkem kui talirapsil (vastavalt 19 296 ja 6 649 isendit). Kahjuriliikide võrdluses oli mõlemal kultuuril ülekaalukalt arvukam naeri-hiilamardikas (Meligethes aeneus). Kultuuride võrdluses oli suvirapsil seda kahjurit 5,9 korda rohkem kui talirapsil. Teine arvukam ristõielistele spetsialiseerunud putukas oli kõdra-peitkärsakas (Ceutorhynchus assimilis), kuid vastupidiselt naeri-hiilamardikale oli tema arvukus suvirapsil 6,9 korda väiksem kui talirapsil (I, II, III).

Kollastest vesipüünistest leiti kuude ülemsugukonda ja 18 sugukonda kuu- luvaid kiletiivalisi parasitoide. Nende hulgas oli neli naeri-hiilamardika parasitoidi: Diospilus capito, Phradis morionellus, P. interstitialis ja Tersi- lochus heterocerus ning kolm kõdra-peitkärsaka parasitoidi: Stenomalina gracilis, Mesopolobus morys ja Trichomalus perfectus. Nagu võis eeldada peremees-putukate arvulisest suhtest (naeri-hiilamardikas:kõdra peitkär- sakas) oli naeri-hiilamardika parasitoidide isendiline arvukus tunduvalt suurem kui kõdra-peitkärsaka parasitoidide oma. Sarnaselt peremeestega oli ka parasitoide arvukamalt suvirapsil kui talirapsil. Parasitoidide liikide omavahelisel võrdlusel oli Diospilus capito kõige arvukam liik nii suvi- kui talirapsil, samas kultuuride võrdluses oli seda liiki suvirapsil 1,4 korda rohkem kui talirapsil. Teine arvukam parasitoid oli Phradis morionellus (I, II, III).

Kuigi kahjuritest oli rapsil ülekaalukalt arvukam naeri-hiilamardikas, on ta meil siiski võtmekahjuriks vaid suvirapsil, talirapsile ilmub ta õitsemise faasis ning olulist kahju ei tekita. Eelkõige on see tingitud talirapsi vara- semast õitsemisest ja pikemast vegetatsiooniperioodist, mis kahjustuse korral tagab ühtlasi ka taimedele parema kompensatsioonivõimaluse. Kõdra-peitkärsakad seevastu olid talirapsiga fenoloogiliselt paremini sünkroniseerunud kui hiilamardikad, sest seal toimus ka nende palju- nemine.

Minimeeritud viljelusviis soodustas naeri-hiilamardika (M. aeneus) ja kõdra-peitkärsaka (C. assimilis) looduslikke vaenlasi nii suvi- kui ka talirapsi põldudel. Naeri-hiilamardika vastsete lahkamine näitas, et parasiteeritud vastsete hulk oli MIN põldudel suurem kui STN põldudel. Minimeeritud viljelusega põldudelt leiti ka kõdra-peitkärsaka parasiteeritud vastseid rohkem kui tavaviljelusega põldudelt. Nii olid suvirapsi minimeeritud põldudelt saadud vastsetest 32% parasiteeritud, samas

33 kui tavaviljeluspõldudelt ei leitud ühtegi parasiteeritud vastset (II, III). Naeri-hiilamardika populatsioon kasvas 2003–2005 aastatel suvirapsil lineaarselt, olles aga alati MIN põldudel madalamal tasemel kui STN põldudel, vaatamata sellele, et STN põldudel kasutati kahjurite tõrjeks insektitsiide (IV).

Kevadel asustasid talvitunud hiilamardikad mõlema süsteemi põlde ühtla- selt. STN põldude töötlemine putukamürkidega vähendas hiilamardikate arvukust siis, kui töötlemine viidi läbi rapsitaimede kõige haavatava- mas kasvustaadiumis – rohelise punga staadiumis. See andis rapsitaimedele STN põldudel võimaluse produtseerida märkimisväärselt rohkem õisi kui MIN põldudel, kus kahjurid rapsi õiepungi hävitasid. Seega pakku- sid STN põldude rapsitaimed edaspidi hiilamardikatele rohkem võima- lusi toitumiseks ja munemiseks kui MIN põldude rapsitaimed. Järelikult mõjutasid viljelussüsteemid rapsitaimede arhitektuuri ning STN süs- teemi taimed said kasvatada rohkem õisi kui MIN süsteemi taimed, mis omakorda viis kahjurite arvukuse suurenemisele STN süsteemis.

Hiilamardikate uue põlvkonna arvukus oli aastate lõikes varieeruv. Kõige enam oli neid STN põldudel 2005. aastal, ning see erines oluliselt kahest eelnevast aastast (IV). Ka Hokkanen (2000) on leidnud, et insektitsiididega töötlemine ei vähenda oluliselt hiilamardika uue põlvkonna arvukust, küll aga aitab töötlemine kaitsta ja suurendada jooksva aasta rapsi- saaki. Käesolev uurimistöö näitas, et insektitsiididega töötlemine hoopis suurendas hiilamardikate uue generatsiooni arvukust (IV). Kuivõrd aga nii parasitoidide arvukus kui ka kahjurite parasiteerituse tase olid suurem MIN põldudel, siis on loogiline järeldada, et insektitsiidid hävitasid STN põldudel ka kahjurite arvukust vähendavad kasulikud organismid. Seevastu MIN põldudel vähendasid nii parasitoidid kui ka röövtoiduli- sed lülijalgsed hiilamardikate uue põlvkonna arvukust.

Mullaharimisel on suur mõju nii mullapinnal kui mullas elavale fau- nale. Tavasüsteemides vähendab nii sügiskünd kui ka kevadine inten- siivne mullaharimine põllul talvituvate parasitiodide ja röövtoiduliste lülijalgsete hulka, aga pärsib ka nende kevadist paljunemist ja arengut. Kui vähendada mehhaanilist põlluharimist, annab see võimaluse sega- matult tegutseda nii mulla kui ka mullapinna elustikul. Kõrdekülv ja minimeeritud mullaharimine säästavad kasureid, kes oma elutegevusega vähendavad kahjurite survet.

34 ACKNOWLEDGEMENTS

The study was carried out at the Institute of Agricultural and Envi- ronmental Sciences, Estonian University of Life Sciences. First of all, I would like to thank my supervisors Anne Luik and Luule Metspalu and also Ingrid Williams from Rothamsted Research, UK for their support and encouragement during the study and for valuable comments and suggestions during the study period and throughout the preparation of the manuscript.

I am greatly indebted to Reelika Kevväi for her help and contribution during these study years. I am very grateful to all my colleagues and friends at the department of plant protection for their help and fruitful discussions: Merje Toome, Maris Saarniit, Külli Hiiesaar, Marika Mänd, Eda Koskor and Reet Karise. My special thanks belongs to Tiiu Kull for her constant support in so many various ways.

I am very thankful to my husband Peeter, and our daughters Linda-Liisa and Kai-Riin for their affection, patience, encouragement and help with ﬁeld work during these study years. I also thank my parents, sister and all my friends.

I warmly thank the publishing house Eesti Loodusfoto for all-around support, their beautiful work and contribution to improving the appear- ance of my thesis.

Thanks to all the partners of the EU project MASTER. I highly ap- preciate the experience, valuable knowledge, and information I gained in the workshops of this project and in the ﬁeld- and laboratory work at Rothamsted Research.

This study was supported by the Estonian Science Foundation (Grants No 4993, 5736, 6722 and SF0172655s04).

35 36 I

PUBLICATIONS 38 © Entomologica Fennica. 8 December 2006

Key pests and their parasitoids on spring and winter oilseed rape in Estonia

Eve Veromann, Anne Luik, Luule Metspalu & Ingrid Williams

Veromann, E., Luik, E., Metspalu, L. & Williams, I.: Key pests and their parasitoids on spring and winter oilseed rape in Estonia. — Entomol. Fennica 17: 400–404. The pests and their hymenopterous parasitoids present in a spring and a winter oilseed rape crop in Estonia were studied. Meligethes aeneus was the most abundant pest in both crops. Other crucifer-specialist pests included: Ceutorhynchus assimilis, C. pallidactylus, C. rapae, C. floralis, C. pleurostigma and Phyllotreta spp., but their abundance was low. Four species of parasitoids of M. aeneus larvae (Diospilus capito, Phradis morionellus, P. interstitialis and Tersilochus heterocerus) and three of C. assimilis larvae (Mesopolobus morys, Stenomalina gracilis and Trichomalus perfectus) were also found. Eve Veromann, Anne Luik and Luule Metspalu, Department of Plant Protection, Estonian Agricultural University, Kreutzwaldi 64, Tartu 51 014, Estonia; corre- spondent author’s e-mail: [email protected] Ingrid Williams, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK Received 9 March 2005, accepted 21 February 2006

1. Introduction ticularly on spring oilseed rape (Alford et al. 2003). All of these pest species are attacked by The expansion of area of oilseed rape (Brassica hymenopterous parasitoids, notably from the fa- napus L.) grown in Europe has resulted in an in- milies Braconidae, Ichneumonidae, and Ptero- crease in the number of pests (Büchi 1996, Cook malidae that attack the larvae, and these are being et al. 1999, Hokkanen 2000). In Estonia, the area exploited for bio-control in integrated pest man- sown to the crop has increased greatly over the agement strategies (Williams et al. 2003a). For last decade, with 50,400 hectares grown in 2004 example, M. aeneus is attacked by nine species of (Statistics Board 2005). parasitoids (Nilsson 2003). Of these Phradis The major pests of winter oilseed rape in Eu- morionellus (Holmgren) (Hymenoptera, Ichneu- rope are Meligethes aeneus (Fabricius) (Coleop- monidae) and Diospilus capito (Nees) (Hyme- tera, Nitidulidae), Ceutorhynchus assimilis (Pay- noptera, Braconidae) are the most important, and kull), C. pallidactylus (Marsham), C. napi Gyl- in Switzerland, over 60% of larvae have been re- lenhal (Coleoptera, Curculionidae), Dasineura ported parasitized (Billqvist & Ekbom 2001a). brassicae (Winnertz) (Diptera, Cecidomyiidae) Ceutorhynchus assimilis is attacked by over 30 and Psylliodes chrysocephala (Linnaeus) (Cole- species of parasitoids (Williams 2003), of which optera, Chrysomelidae) (Alford et al. 2003, Wil- Trichomalus perfectus (Walker) (Hymenoptera, liams 2004). Flea beetles (Phyllotreta spp. Cole- Pteromalidae) is the most widespread, abundant optera, Chrysomelidae) are also important, par- and important (Williams 2003). The most impor-

39 ENTOMOL. FENNICA Vol. 17 • Key pests and parasitoids on oilseed rape 401 tant parasitoids of C. pallidactylus are Tersi- were positioned at the top of the crop canopy and lochus obscurator Aubert, T. tripartitus Brisch- raised weekly to keep pace with crop growth. In- ke,T. exilis Holmgren (Hymenoptera, Ichneu- sects were collected from them once a week until monidae), and Stibeutes curvispina (Thomson) harvest. The samples were sorted, phytophagous (Hymenoptera, Ichneumonidae) (Ulber 2003, crucifer-specialist insects and all hymenopterous Barari et al. 2004). parasitoids were separated and stored in 70% eth- In Estonia, knowledge of rape pests and of anol at –18°C, for later identification and count- their hymenopterous parasitoids is fragmentary ing of key species. and largely confined to the description of species. The aim of this study was to identify the key pests and their parasitoids on winter and spring rape in 3. Results and discussion Estonia and to compare the species composition on the two crops. This information is essential to 3.1. Winter rape 2002 underpin the development of economically-viable and ecologically-sustainable rape cultivation Only two of the most important of the European technologies. pests were caught in the traps, M. aeneus and C. assimilis, of which the former was the more abundant (Table 1). Meligethes viridescens and 2. Material and methods C. floralis were also relatively abundant. Two species of Phyllotreta (P. armoraciae and P. ne- The winter rape crop sampled was the variety morum) were caught in low numbers, and only “Hansen”, grown at Puki Farm, Tartu County in one specimen of C. rapae Gyllenhal was caught. 2001/2. The study field (4 ha) was approximately Although Phyllotreta species are important pests rectangular, bordered to the north by winter of cruciferous plants, they do not usually cause wheat, to the east by natural meadow and to the much damage to winter rape, appearing when south and west by gravel road. The previous crop plants are well established and have already was clover. The spring rape crop sampled was the formed bud rosettes. The relatively large numbers variety “Quantum” grown at Pilsu Farm, Tartu of C. floralis caught were unexpected, as this spe- County in 2003. It followed winter wheat. The cies is not widespread or abundant on cultivated study field (4 ha) was rectangular and bordered to crucifers preferring wild cruciferous plants the north by an asphalt road, with a 10 m strip of (Metspalu & Hiiesaar 2002). It was the earliest barley between the road and the rape, to the south pest to arrive appearing at mid-flowering (BBCH by winter wheat, to the west by grassland and to 65-66). Meligethes spp. and C. assimilis were the east by barley. The soil was loamy in both first caught at the end of flowering, and remained fields (average pH KCI 6.15). the dominant species thereafter, with greatest Insects were sampled using yellow water numbers during pod development (BBCH 71- traps (210 × 310 × 90 mm). Yellow water traps 72). have been used extensively to sample pests and Although the numbers of M. aeneus were their parasitoids in oilseed rape (Williams et al. large, they arrived when the plants were mostly 2003b). Yellow is the most effective colour for past the bud stage suitable for oviposition. Al- trapping them. Traps placed at the top of the can- though C. assimilis was also abundant in the opy are particularly effective for sampling insects traps, no larval damage to the pods was found, that fly within the upper canopy e.g. the inflores- suggesting that the synchrony of this species with cence pest M. aeneus and C. assimilis and their crop growth was poor, and that it arrived at a sex- parasitoids, but not as effective for stem-mining ually-immature stage or when the crop was un- pests and their parasitoids, which fly lower in the suitable for egg-laying. This species was there- canopy. Ten traps were placed in the winter rape fore not an important pest of winter rape that year. in the beginning of flower (BBCH 61-62 of Meier Yellow water trap catches contained hyme- (2001)) on 8.V.2002, and on the spring rape at nopterous parasitoids from six superfamilies and BBCH 0 (14.V.2003), just after sowing. They from 16 families. However, the numbers of those

40 402 Veromann et al. • ENTOMOL. FENNICA Vol. 17

Table 1. Total numbers of crucifer-specialist insects and their parasitoids caught in yellow water traps (N=10) in 2002–2003 on winter and spring rape at Puki and Pilsu Farm, Tartu County, respectively.

Pest/Parasitoid Winter oilseed rape Spring oilseed rape

Meligethes aeneus (Coleoptera, Nitidulidae) 1,118 2,246 Diospilus capito (Hymenoptera, Braconidae) 0 7 Phradis morionellus (Hymenoptera, Ichneumonidae) 1 64 Phradis interstitialis (Hymenoptera, Ichneumonidae) 0 26 Tersilochus heterocerus (Hymenoptera, Ichneumonidae) 0 1 Meligethes viridescens (Coleoptera, Nitidulidae) 290 64 Ceutorhynchus assimilis (Coleoptera, Curculionidae) 649 67 Trichomalus perfectus (Hymenoptera, Pteromalidae) 1 3 Mesopolobus morys (Hymenoptera, Pteromalidae) 1 1 Stenomalina gracilis (Hymenoptera, Pteromalidae) 1 0 Ceutorhynchus floralis (Coleoptera, Curculionidae) 251 6 Ceutorhynchus rapae (Coleoptera, Curculionidae) 1 100 Ceutorhynchus pallidactylus (Coleoptera, Curculionidae) 0 1 Tersilochus tripartitus (Hymenoptera, Ichneumonidae) 0 4 Phyllotreta spp. (Coleoptera, Chrysomelidae) 4 101

that attack the pests of oilseed rape were very low pods were beginning to ripen (BBCH 80-81), in- with only one specimen of each of four species, dicating emergence of the new generation from namely, P. morionellus, which attacks M. aeneus the soil. Few C. assimilis were caught. Probably larvae and T. perfectus, M. morys and S. gracilis by the time spring rape had reached the young (Hymenoptera, Pteromalidae) which attack C. pod growth stage suitable for egg-laying by this assimilis larvae (Table 1) caught. This paucity of weevil, it had already laid its eggs on other suit- parasitoids in the crop is surprising. Phradis able cruciferous plants. Ceutorhynchus rapae morionellus is recognised as an abundant and ef- was relatively numerous; this species is not con- fective regulator of its host in Scandinavia sidered to be a pest of oilseed rape, feeding (Billqvist & Ekbom 2001a). In the Uppland re- mainly on cabbage, radish and turnip. A few C. gion of Sweden, parasitism levels of 56% by P. floralis were also caught. morionellus and 29% by D. capito in M. aeneus Of parasitoids of M. aeneus, P.morionellus, P. larvae have been reported (Billqvist & Ekbom interstitialis, D. capito and T. heterocerus were 2001a,b). Herrström (1964) found, at one loca- caught on spring rape. Both Phradis spp. were tion in Sweden, 100% parasitism of C. assimilis caught during flowering when host larvae were larvae with M. morys as the dominant parasitoid. abundant in the flowers. Diospilus capito, a multivoltine braconid endoparasitoid, appeared in catches as pods began to ripen (BBCH 80-81) 3.2. Spring oilseed rape 2003 and as the new generation of M. aeneus emerged. Diospilus capito, P. morionellus, P. interstitialis As on winter rape, the most abundant pest species and T. heterocerus have all been recorded in Fin- was M. aeneus (Table 1). The first were caught on land (Hokkanen 1989), at the northern distribu- the crop at the two-leaf stage, although more tion limit of oilseed rape cultivation. Of the commonly they arrive later when flower buds are parasitoids of C. assimilis, only a few M. morys, present (Nilsson 1988). Their numbers increased and T. perfectus were caught. Afew T. tripartitus, steadily to a maximum at first flower (BBCH 59- a solitary, univoltine, ichneumonoid endopara- 60) and then decreased again as flowering fin- sitoid of P. chrysocephala and C. pallidactylus ished. A new increase in numbers occurred as were also caught.

41 ENTOMOL. FENNICA Vol. 17 • Key pests and parasitoids on oilseed rape 403

3.3. Comparison of the species composition tance in other European rape-growing areas do on spring and winter oilseed rape not yet appear to have reached pest status in Esto- nia, where the crop is relatively new, although The species spectrum of the oligophagous pests many potential pests are present. They may be of winter and spring rape was similar (Table 1), surviving on wild relatives of Brassica crops and but their flight phenologies differed. The most may adapt in time to synchronise their life cycles abundant pest on both crops was M. aeneus, with with that of oilseed rape. Parasitoids of key pest twice as many caught on spring rape as on winter species were present, albeit in low numbers. rape. Similar results were obtained by Šedivy and However, their abundance may increase as the Vašek (2002). Meligethes viridescens was nu- abundance of pests increases with implications merous on winter rape but not on spring rape. for their value in the development of pest man- Conversely, the numbers of C. assimilis caught agement strategies incorporating bio-control. on winter rape were 10-fold those on spring rape. They emerged in spring and used the winter rape Acknowledgements. This research was supported by Esto- for maturation feeding. Ceutorhynchus floralis nian Science Foundation grant no. 4993 and 5736, and the EU Framework 5 Project MASTER (QLK5-CT-2001- was more abundant on winter than on spring rape. 01447). Rothamsted Research receives grant-aided sup- According to the literature, this species is an early port from the Biotechnology and Biological Sciences Re- spring species, which passes through its develop- search Council of the UK. ment cycle on spring weeds. Both C. rapae and Phyllotreta spp., represented only by a few individuals on winter rape, were more abundant on References spring rape. There are several reasons for the differences Alford, D. V., Nilsson, C. & Ulber, B. 2003: Insect pests of in incidence of pests on spring and winter rape. oilseed rape crops. — In: Alford, D. V. (ed.), Bio- One important reason is that the phenological de- control of Oilseed Rape Pests: 8–39. Blackwell Sci- ence, Oxford. velopment of the crop may be asynchronous with Barari, H., Cook, S. M. & Williams, I. H. 2004: Rearing the development of the pests. This can be influ- and identification of the larval parasitoids of Psylli- enced greatly by weather conditions of the year. odes chrsysocephala and Ceutorhynchus pallidac- For example, in a dry and warm spring, winter tylus from field-collected specimens. — IOBC/wprs rape may complete flowering too early to provide Bull. 27(10): 265–274. flower buds for M. aeneus oviposition. Similarly, Billqvist, A. & Ekbom, B. 2001a: The influence of host plant species on parasitism of pollen beetles (Meli- for C. assimilis, winter rape may be past its opti- gethes spp.) by Phradis morionellus. — Entomol. mal growth stage for oviposition by the time the Exp. Appl. 98 (1): 41–47. pest arrives on the crop. Further, hibernating in- Billqvist, A. & Ekbom, B. 2001b: Effects of host plant spe- sects may be killed by severe winter conditions so cies on the interaction between the parasitic wasp that emerging populations may be too small to Diospilus capito and pollen beetles (Meligethes spp.). — Agricultural and Forest Entomology 3: 147–152. damage the crop. The diversity and abundance of Büchi, R. 1996: Eiablage des Rapsstengelrüblers Ceuto- parasitoids, like that of their hosts was greater on rhynchus napi Gyll., in Abhängigkeit der Stengel- spring than on winter rape. länge bei verschiedenen Rapssorten. — Anzeier für Schädlingskunde Pflanzenschutz Umweltschutz 69: 136–139. Cook, S., Murray, D. A. & Williams, I. H. 1999: Pollen 4. Conclusions beetle, Meligethes aeneus Fabricius, incidence in the composite hybrid winter oilseed rape, Synergy. — From this study, we conclude that, in Estonia in Proc. of the 10th international Rapeseed Congress, 26– 2003, M. aeneus was the only key pest and only 29 September 1999, Canberra, Australia. on spring oilseed rape. Other studies have also Herrström, G. 1964: Untersuchungen über Parasiten von shown that winter rape is less vulnerable than Ölfruchtschädlingen in Schweden. — Statens Växt- skyddsanstalt Meddelanden 12: 437–448. spring rape, partly due to earlier flowering, partly Hokkanen, H. 1989: Biological and agrothechnical control due to a longer growth season to compensate for of the rape blossom beetle Meligethes aeneus (Col., attacks (Tarang et al. 2004). Other pests of impor- Nitid.). — Acta Entomol. Fennica 53: 25–29.

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Hokkanen, H. M. T. 2000: The making of a pest: recruit- vils. Chapter 5 — In: Alford, D.V. (ed.), Biocontrol of ment of Meligethes aeneus onto oilseed Brassicas. — Oilseed Rape Pests: 87–95. Blackwell Science, Ox- Entomol. Exp. Appl. 95: 141–149. ford. Meier, U. (ed.) 2001: Growth stages of mono- and di- Williams, I. H. 2003: Parasitoids of cabbage seed weevil. cotyledonous plants. 2nd ed. — [www document] URL Chapter 6. — In: Alford, D.V.(ed.), Biocontrol of Oil- www.bba.de/veroeff/bbch/bbcheng.pdf seed Rape Pests: 97–112. Blackwell Science, Oxford. Metspalu, L. & Hiiesaar, K. 2002: Ristõieliste kultuuride Williams, I. H. 2004: Advances in Insect Pest Management kahjurid. — EPMÜ Taimekaitse Instituut, Tartu. 102 of Oilseed Rape in Europe. — In: Horowitz, A. R. & pp. Ishaaya, I. (ed.), Insect Pest Management: Field and Nilsson, C. 1988: The pollen beetle (Meligethes aeneus F.) Protected Crops: 181–208. Springer-Verlag, Heidel- in winter and spring rape at Alnarp 1976–1978. — berg. Växtskyddsnotiser 52: 139–144. Williams, I. H., Büchs, W., Hokkanen, H., Menzler-Hok- Nilsson, C. 2003: Parasitoids of Pollen Beetles. — In: Al- kanen, I., Johnen, A., Klukowski, Z., Luik, A., ford, D. V. (ed.), Biocontrol of Oilseed Rape Pests: Nilsson, C. & Ulber, B. 2003a: Management strategies 73–85. Blackwell Science, Oxford. for winter oilseed rape pests to enhance bio-control of Statistics Board 2005: — [www document] Cited 3 Oct. th 2005. Updated 22 July 2005. URL http://pub.stat.ee rape pests. — Proc. of the 11 International Rapeseed Šedivy, J. & Vašek, J. 2002: Differences in flight activity of Congress, 6–10 July 2003, Copenhagen, Denmark: pests on winter and spring oilseed rape. — Plant Pro- 1011–1013. tection Science 38 (4): 139–144. Williams, I. H., Büchi, R. & Ulber, B. 2003b: Sampling, Tarang, T., Veromann, E., Luik, A. & Williams, I. H. 2004: trapping and rearing oilseed rape pests and their On the target entomofauna of an organic oilseed rape parasitoids. — In: Alford, D. V. (ed.), Biocontrol of field in Estonia. — Latvias Entomologs 41: 100–110. Oilseed Rape Pests: 145–160. Blackwell Science, Ox- Ulber, B. 2003: Parasitoids of Ceutorhynchid Stem Wee- ford.

43 44 II 46 AGRICULTURAL AND FOOD SCIENCE

Vol. 15 (2006): 161–72.–000.

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: [email protected] 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

pests of oilseed rape are Meligethes aeneus (Fab.), Introduction Meligethes viridescens (Fab.) (pollen beetles), Ceutorhynchus assimilis (Payk.) (cabbage seed In Estonia, the cultivation of oilseed rape (Brassi- weevil), Ceutorhynchus pallidactylus (Marsham) ca napus L., Brassica rapa L.) has expanded great- (cabbage stem weevil), Ceutorynchus napi Gyll. ly in recent years and now exceeds 46,300 ha (Sta- (rape stem weevil), Dasineura brassicae (Winn.) tistics Board 2003). This provides good potential (brassica pod midge), Psylliodes chrysocephala for population growth of crucifer-specialist, phy- (L.)(cabbage stem ﬂea beetle) and Phyllotreta tophagous pests. In Europe, the most common nemorum (L.), Phyllotreta undulata (L.) and Phyl-

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Veromann, E. et al. Oilseed rape insects in Estonia lotreta diademata (L.) (flea beetles) (Alford et al. now than formerly. The occurrence of carabids is 2003). greatly influenced by the farming system, being The management of pests on oilseed rape greater in extensively-managed than in intensive- throughout Europe still relies heavily on chemical ly-managed crops (Hokkanen and Holopainen pesticides, most often applied routinely and pro- 1986, Büchs 2003b). phylactically, often without regard to pest inci- Recent advances in the management of oilseed dence (Williams 2004). This leads to the over-use rape pests have emphasised the important role of of pesticides, which reduces the economic com- natural enemies within integrated pest manage- petitiveness of the crop and threatens biological ment systems for the crop (Williams 2004). The diversity. The pesticides also kill the natural agents EU-funded project MASTER: MAnagement of biological control, which would be a natural re- STrategies for European Rape pests aims to de- source of great potential benefit to the farmer and velop economically-viable and environmentally- the consumer (Alford et al. 1995, Williams and acceptable crop management strategies for winter Murchie 1995). By killing natural enemies, pesti- oilseed rape which maximise the biological con- cide applications must be increased further to trol of key pests and minimise chemical inputs achieve pest control (Pickett et al. 1995, Murchie (Williams et al. 2002). This requires much greater et al. 1997). Parasitoids can control the pests. For knowledge of pest, parasitoid and predator taxon- example, more than 30 species of hymenopterous omy and biology throughout Europe. In Estonian parasitoids have been reported to attack C. assimi- conditions, the pests of oilseed rape and their natu- lis in Europe (Williams 2003). Of these, the larval ral enemies have been little studied. The present ectoparasitoid Trichomalus perfectus Walker (Hy- pilot study aims to add to knowledge of rape pests menoptera: Pteromalidae) is widely distributed and their natural enemies in Estonia and contrib- and particularly important (Lerin 1987, Murchie utes to the project MASTER. and Williams 1998a). In addition to killing larvae The aim of this pilot study was to compare the through direct parasitism, it further kills by host effects of minimised (no plough, direct drilling, no feeding, and reduces damage to infested pods by pesticides) and standard (plough, standard applica- preventing host larvae from eating their full com- tion of pesticides) cropping systems on oilseed plement of seeds (Murchie and Williams 1998b). rape plant architecture and the occurrence of pests, Host selection by parasitoids may be influenced by their hymenopteran parasitoids and carabid preda- plant characteristics (Vinson 1976) and plant ar- tors. 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 Material and methods (Büchs 2003a). In oilseed rape fields, the dominant predators are carabids, these having the greatest The study site biomass in comparison with rove beetles and spi- ders (Goltermann 1994). They are present all year The study compared a minimised (MIN) with a round and can suppress pest populations at an ear- standard (STN) system of cropping spring oilseed ly stage (Büchs 2003a). Over 20 species of carabid rape in 2003. The study site comprised two adja- occur regularly in European oilseed rape fields. cent, approximately rectangular fields (both 2 ha) The species’ composition within communities var- on Pilsu Farm, Tartu County, Estonia (58°14´ lati- ies from country to country and also from site to tude 26°16´ longitude). The soil was loamy (aver- site, according to regional or local conditions; age pH KCI 6.15). In both fields, spring oilseed changes have also occurred over time, with larger rape cv. Quantum (seeding rate 6 kg ha-1) was species (e.g. Carabus spp.) being less abundant drilled on 12 May, following winter wheat.

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In the STN system, ploughing and pesticides Insect samples were sorted and target taxa were used. The herbicide Treflan Super (2 l ha-1) identified and counted in the laboratory. The cruci- was applied before drilling, and the herbicide fer-specialists, hymenopterous parasitoids and Lontrel 300 (0.3 l ha-1) was applied at the two-leaf ground beetles were separated and stored in 70% growth stage (BBCH-stage) (BBCH 12 of Meier ethanol at –18°C. The target phytophagous insects (2001), Lancashire et al. (1991)). The fungicide and carabids were identified to species. Hymenop- Folicur (1 l ha-1) was applied at BBCH 50–51 and terous parasitoids were identified to family, except the insecticide Fastac (0.15 l ha-1) at BBCH 65–66. those specialised on the target phytophagous in- In the MIN system, direct drilling replaced plough- sects, which were identified to species. ing and no pesticides were used. The fields were bordered to the north by an asphalt road, with a 10 m strip of barley between the Plant sampling road and the oilseed rape, to the south by winter wheat, to the west by grassland and to the east by a The growth stages of the rape plants in both crops crop of barley. The MIN field had many weeds, were recorded weekly using the Meier (2001) key. dominated by Tripleurospermum inodorum (L.), Plant density, architecture and infestation and Stellaria media (L.) and Galeopsis tetrahit L. In damage by pests were also determined in both the STN field, Capsella bursa-pastoris (L.) was crops. Oilseed rape plant and weed density per m2 abundant. was determined from 5 randomly-selected places In 2003, spring/summer weather was warmer in both fields on two occasions (BBCH 12 and and wetter than average. Data from the local mete- 69–71). Plant architecture and pest infestation was orological station at Eerika, near Tartu showed that determined on 10 plants from 5 randomly-chosen May temperatures (mean 11.6°C) were 1.4°C and locations (50 plants from STN and 50 from MIN) July temperatures (mean 19.4°C) were 1.5°C collected on 21 August (BBCH 83). Each plant warmer than the long-term average. Rainfall in was measured (stem height and diameter and the May (mean 142.8 mm) was 2.3 times greater, and number of pods and podless stalks on the main ra- in August (mean 132.8 mm) almost 2 times greater ceme and side branches). Damage caused by M. than the long term average. The warm, moist aeneus was assessed as the number of podless spring promoted the growth and development of stalks (podless stalks in the very top of the stem the rape crop whereas the wet August inhibited were not counted because this may have been crop ripening and harvesting. caused by other factors, e.g. lack of pollination. Stems were dissected for C. pallidactylus larval mining damage. Pods were examined for the pres- Insect sampling ence of live or dead C. assimilis and D. brassicae larvae, the exit holes of emerged C. assimilis lar- Insects were sampled using water and pitfall traps vae or those of its ectoparasitoids or pod shatter emptied weekly from post-drilling (14 May) to pre- due to D. brassicae larvae. 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. Statistical analysis They were positioned at the top of the crop canopy to sample flying insects and raised weekly, as nec- Although only one field with each cropping sys- essary, to keep pace with crop growth. Four were tem was observed the data were analysed using the placed within the crop 15 m from different borders following statistical methods because all other and two were placed outwith the crop. Pitfall traps conditions in the two fields were similar. Statistical for sampling carabids were placed along a central analysis used SAS GLM and GENMOD proce- transect of each field (5 in STN and 5 in MIN). dures. The differences of means of plant parame-

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Veromann, E. et al. Oilseed rape insects in Estonia ters and the numbers of oilseed rape and weed STN, mean 91.3 per m2), as well as later, (BBCH plants per m2 were compared with analysis of vari- 69–71), however, there were significantly more ance. Comparisons of the numbers of pests, parasi- weeds in the MIN field (P = 0.0015) (Fig. 1). The toids and carabids were made using type 3 empiri- dominating weed was T. inodorum. cal standard errors analysis and the Poisson distri- Stem height, stem diameter and the number of bution and the log link function. The numbers of side branches were similar in the MIN and the pests and carabids caught each week were also STN crop. However, main raceme and side branch- analysed separately. For analyses of the numbers es of the MIN plants had significantly (P = 0.043 of carabids the scale parameter was estimated by and P = 0.0016) fewer pods than those of the STN Pearson’s Chi-Square divided by the degrees of plants (Fig. 2). Damage by M. aeneus, assessed as freedom because of overdispersion of the model. podless stalks, was less in the STN than in the MIN field (Fig. 2). Few pods were damaged by C. assimilis 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 Results infestation by D. brassicae was found. Plant density, architecture and pest damage

No Median; Box: 25%, 75%; Whisker: Min, Max Plant density was similar in both crops, early in 260 development (BBCH 12; MIN, mean 86.3 per m2;

220

No in m 2 Median 90 180

ANOVA: Weeds: F(1,8)=22, P=0.0015 Oilseed rape: F(1,8)=1.86, P=0.21 140 70 N=5

100

50 60

30 20

-20 10 STN MIN

ANOVA: Pods on main raceme Main raceme: Podless stalks F(1,98)=4.19, P=0.043 -10 Pods on side branch STN MIN Side branches: F(1,98)=10.6, P=0.0016 Min, max Podless stalks: 25%, 75% F(1,98)=15.93, P=0.00013 Oilseed rape N=50 Weeds Fig. 2. The median number of podless stalks on the main Fig. 1. The median number of oilseed rape plants (BBCH raceme, of pods on the main raceme and on side branches 69–71) and weeds per m2 in standard (STN) and minimised on rape plants grown using a standard cropping system cropping system (MIN) ﬁelds on Pilsu Farm, Tartu Coun- (STN) and a minimised cropping system (MIN) on Pilsu ty, Estonia in 2003. Farm, Tartu County, Estonia, in 2003.

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Pest incidence and phenology lation peaks, on 2 July and 13 August. The first peak coincided with first flower (BBCH 59–60). During the study, 60 samples with a total of 2,588 The second occurred during pod ripening (BBCH specimens of crucifer-specialist insect pests from 80–81). At both peaks and throughout the study eight taxa (Table 1) were collected from the water period, M. aeneus abundance was greater in the traps (MIN, 792 specimens; STN 1,796 speci- STN field than in the MIN field (Fig. 4, �² = 11.04, mens). df = 1, P = 0.0009). Meligethes aeneus started to colonise the Ceutorhynchus assimilis abundance was low oilseed rape from BBCH 12 (Fig. 3), increasing on both crops (Fig. 4). The first were found on 12 from 12 June (BBCH 14) and showing two popu- 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

No Median; Box: 25%, 75%; Whisker: Min, Max 400

350 STN MIN 300 N = 4 250 *

200

150

100 * Fig. 3. The median numbers of * * Meligethes aeneus per yellow 50 water trap caught at different growth stages (BBCH) in stand- 0 ard (STN) and minimised (MIN) -50 cropping system ﬁelds of spring oilseed rape on the Pilsu Farm, 1.06 0/21.05

Tartu County, Estonia, in 2003 (* 14/1 10/28.05 12/04.06 80/06.08 50-51/25.06 63-65/09.07 82-83/20.08 87-89/27.08 30-31/18.06 59-60/02.07 65-66/16.07 69-71/23.07 79-80/30.07 indicates signiﬁcant difference 80-81/13.08 between systems). BBCH/Date

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No Median; Box: 25%, 75%; Whisker: Min, Max 9

STN MIN 7 N = 4

5 * * 3 *

Fig. 4. The median numbers of 1 Ceutorhynchus assimilis per yellow water trap caught at different rape growth stages (BBCH) in -1 standard (STN) and minimised 5 (MIN) cropping systems ﬁelds of 1.06 spring oilseed rape on Pilsu Farm, 0/21.0 10/28.05 12/04.06 14/1 80/06.08 Tartu County, Estonia, in 2003 (*

30-31/18.06 50-51/25.06 59-60/02.07 63-65/09.07 65-66/16.07 69-71/23.07 79-80/30.07 80-81/13.08 82-83/20.08 87-89/27.08 indicates signiﬁcant difference BBCH/Date between systems).

peaks, the first at first flower (BBCH 59–60) and toids, D. capito, P. morionellus, P. interstitialis and the second during pod maturation (BBCH 79–80). T. heterocerus, totals of 47 and 51 specimens were Abundance was greater in the STN field than in the found in the STN and the MIN field, respectively. MIN field (Fig. 5, �² = 26.02, df = 1, P < 0.0001). 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- Parasitoid incidence and phenology dance of D. capito, the endoparasitoid of M. aeneus larvae, coincided with peak abundance of Hymenopteran parasitoids from six superfamilies new generation M. aeneus (BBCH 80–83). Peak and 18 families were captured in the water traps abundance of P. morionellus, P. interstitialis and T. (MIN, 828 specimens; STN, 660 specimens). heterocerus, coincided with M. aeneus colonisa- Amongst them were four parasitoids of M. aeneus: tion. A total of only three specimens of T. perfec- Diospilus capito, Phradis morionellus, Phradis in- tus, and one specimen of M. morys, both ectopara- terstitialis and Tersilochus heterocerus and two sitoids of C. assimilis larvae, were found. parasitoids of C. assimilis: Mesopolobus morys and T. perfectus (Table 2). The number of parasitoids increased as the Carabid incidence and phenology rape started to flower (BBCH 59–60). At full flower, numbers were greater in the STN than in MIN During the study, 150 pitfall trap samples were field (Fig. 5). The parasitoid population reached collected, containing a total of 3,045 carabids. Ac- maximum during pod ripening (BBCH 79–80) in tivity-density was greater in the MIN than in the the MIN field. The numbers of key parasitoids STN field (from MIN 2169 and STN 876 speci- caught from the two cropping systems were simi- mens; �² = 6.27; df = 1; P = 0.0123) (Table 3). In lar and not large. Of the M. aeneus endoparasi- the MIN field, maximal activity-density of cara-

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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

No Median; Box: 25%, 75%; Whisker: Min, Max 160

140 STN 120 MIN N=4 100

20 Fig. 5. The median numbers of hymenopteran parasitoids per 0 yellow water trap caught at different rape growth stages (BBCH) -20 in standard (STN) and minimised 1.06 (MIN) cropping system ﬁelds of 0/21.05 14/1 10/28.05 80/06.08 spring oilseed rape on the Pilsu 12/04.06 87-89/27.08 65-66/16.07 80-81/13.08 82-83/20.08 30-31/18.06 69-71/23.07 50-51/25.06 63-65/09.07 79-80/30.07 Farm, Tartu County, Estonia, in 59-60/02.07 2003. BBCH/Date

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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 Meligethes aeneus was by far the most numerous (BBCH 69) (Fig. 6). The three most abundant spe- and the only one to reach pest status. The second cies in both the MIN and the STN fields were most abundant pest was C. assimilis. A few M. Pseudoophonus rufipes, Poecilus cupreus and viridescens were also caught; this species requires Pterostichus melanarius. Pseudoophonus rufipes higher temperatures for oviposition and develop- was the dominant carabid species caught, consti- ment than M. aeneus (Alford et al. 2003). In addi- tuting more than half of all specimens in both tion, Ceutorhynchus rapae, C. floralis, C. pleu- fields. Poecilus cupreus was the second most abun- rostigma and flea beetles (Phyllotreta spp.) were dant species. Both of them were caught signifi- also captured but their abundance was low. Ceuto- cantly more in the MIN than in the STN field (P. rhynchus rapae is infrequently recorded in Estonia rufipes: �² = 5.71; df = 1; P = 0.0169; P. cupreus: (Metspalu and Hiiesaar 2002) and therefore the �² = 5.90; df = 1; P = 0.0151) and their activity- relative large number caught (totally 50, in BBCH density peak coincided with M. aeneus larval drop 12 in STN field) was unusual. Insect incidence on at the end of rape flowering (BBCH 69) (Fig. 6). oilseed rape is dependent on several factors, such as oilseed rape plant architecture, presence of flowering weeds, crop rotations, landscape structure etc. (Walters et al. 2003). Weeds can exert direct stress on crops (by competing for sunlight, Discussion moisture etc.) or affect indirectly through enhancing the presence of the natural enemies of pests During the study, the three major European pests (Altieri and Nicholls 2004). In our study, oilseed of oilseed rape: M. aeneus, C. assimilis and C. pal- rape plant density was similar in both crops but lidactylus (one specimen only) were collected. there were significantly more weeds in the MIN

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No Median; Box: 25%, 75%; Whisker: Min, Max 260 STN MIN 220

N=5 180

140

100

Fig. 6. The median numbers of 60 carabids per pitfall trap caught at different rape growth stages 20 (BBCH) in standard (STN) and minimised (MIN) cropping sys- -20 7 6 7 7 8 8 6 7 8 7 tem ﬁelds of spring oilseed rape 5 on Pilsu Farm, Tartu County, Es- 1.06 0/21.0 10/28.05 12/04.06 14/1 tonia, in 2003 (* indicates signiﬁ- 80/06.08 50-51/25.0 63-65/09.0 82-83/20.0 59-60/02.0 65-66/16.0 79-80/30.0 87-89/27.0 80-81/13.0 69-71/23.0 cant difference between sys- 30-31/18.0 tems). BBCH/Date

field. The weeds were large enough to compete architecture, enabling plants in the STN field to with the crop plants for food and light, probably produce more flowers than those in the MIN field, accounting for the reduction in the number of flow- which in turn resulted in greater infestation by M. ers on the side branches of the rape plants in the aeneus and C. assimilis in the former. MIN compared with the STN field. The greater Parasitoids of both of key pests were found. abundance of rape flowers in the STN field pro- Four parasitoids of M. aeneus: D. capito, P. mori- vided a greater food resource for M. aeneus so onellus, P. interstitialis and T. heterocerus and two their damage to the main raceme was lower in the parasitoids of C. assimilis: M. morys and T. perfec- STN than in the MIN field, where the beetles con- tus were captured. All are recorded for the first centrated on the main raceme on the plants. time in Estonia (Tryapitzyn 1978, Kasparjan The two most numerous pests, M. aeneus and 1981). These parasitoid species are found over C. assimilis, each had two population peaks at ap- most of Europe, from southern Sweden to France proximately the same time, the first at first flower (Nilsson 2003, Williams 2003) with those of M. (BBCH 59–60) and the second during pod ripen- aeneus at the northern distribution limit of oilseed ing (BBCH 80–81). The second peak indicated rape in Finland (Hokkanen 1989). The distribution emergence of the new generation from the soil. and abundance of different species depends on fac- Despite the application of insecticide to the STN tors such as the local climate, the crops grown dur- field at BBCH 65 pest abundance was greater in ing previous years and the cultivation techniques the STN field than in the MIN field throughout the used (Nilsson 2003). At full flower, the number of study period. This could be explained by differ- parasitoids was greater in the STN than in MIN ences in crop performance in the case of M. ae- field, probably attracted by the greater abundance neus, and in the case of C. assimilis, by the greater of flowers; adult parasitoids are exclusively de- resource of young pods for oviposition. The crop- pendent on floral and extrafloral nectar, honeydew ping system appears to have influenced rape plant and pollen for food (Lewis et al. 1998). During

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Veromann, E. et al. Oilseed rape insects in Estonia pod ripening (BBCH 79–80), the further increase lighted the important role of weeds in the presence in the number of parasitoids in the MIN field prob- of predators in the fields. This could be true also ably indicated the emergence of new generations for the present study, where the MIN field with its of some hymenopteran parasitoid species. Key reduced tillage, no pesticides and more weeds of- parasitoid phenology was synchronised with that fered greater food resources for carabids. Maximal of their hosts. Peak abundance of D. capito, coin- activity-density of carabids in the MIN field was cided with peak abundance of new generation M. two weeks before the maximal abundance of the aeneus (BBCH 80–83), indicating that they prob- new generation of M. aeneus. This is the period ably emerged from host larvae in the oilseed rape. when M. aeneus larvae are mature, drop to the soil Diospilus capito is multivoltine with two or three to pupate, and are most vulnerable to predation. generations in northern Europe (Billquist and Ek- The three most abundant species in both fields: P. bom 2001a, Nilsson 2003). The other captured rufipes, P. cupreus and P. melanarius have been parasitoids of M. aeneus have one generation per reported as typical of winter rape fauna (Lang- year and after pupating in the host pupal chamber maack et al. 2001, Luik et al. 2001). According to in the soil stay in diapause in the cocoon until the Thiele (1977), 50% of the food consumed by P. following spring or summer (Nilsson 2003); they rufipes is animal matter. Poecilus cupreus is an im- were found at the same time as M. aeneus colo- portant predator of M. aeneus larvae (Büch 2002). nised. Due to the low abundance of C. assimilis a Similarily to our data, Büchs and Nuss (2000) also very few of its parasitoids were found also. Tri- found strong coincidence between the time of the chomalus perfectus is a univoltine ectoparasitoid occurrence of P. cupreus and P. melanarius and reported, in winter rape, to have an abundance that of oilseed rape pest larvae during their change peak two to four weeks after peak migration of C. of strata for metamorphosis, and suggested that assimilis into the crop. New-generation parasitoids carabids are important larval predators. Predatory mate on emergence and leave the crop shortly be- efficacy is greatly influenced by the time period fore harvest. Only females overwinter, possibly in over which carabids can prey upon M. aeneus lar- evergreen foliage (Williams 2003). In Estonia, the vae. With unlimited access to the larvae during the total number of key parasitoids was very low prob- whole “dropping” period, mortality of larvae can ably because the history of oilseed cropping is be considerable (78%) (Büchs 2003a). Delayed short and the parasitoids may need more time to flowering of the crop, high density of pest larvae build up their populations. Although their greater and longer duration of the larval “dropping” period abundance in the MIN field suggests potential to enhances the positive effects of polyphagous epi- encourage them with more environmentally- gaeic predators in oilseed rape (Büchs 2003a). Al- friendly crop management, but this requires addi- though there was more potential prey (M. aeneus tional research. larvae) in the STN field, there were significantly Beside parasitoids, carabids also have potential fewer carabids in the STN than in the MIN field. to impact rape pest populations through predation. This was probably caused by insecticide treatment, For example, fully-grown larvae of M. aeneus, to which carabids are known to be sensitive. Tu- drop to the ground for pupation, and are then im- ubel and Toom (1999) found that the treatment of portant components of the diet of carabids (Büchs a barley field with Fastac significantly decreased and Alford 2003). The MIN field had greater abun- the numbers of Harpalus and Pterostichus. The dance of carabids than the STN field. This agrees application of Fastac to the STN field (BBCH 65– with the findings of Hokkanen and Holopainen 66) probably killed a proportion of the carabids (1986), Langmaack et al. 2001 and Irmler (2003) either directly or via poisoned prey. Therefore ac- who also found more individuals and species of tivity-density peak of carabids was obvious only in carabids on biologically- or minimally-managed the MIN field, where their pressure on M. aeneus fields, which they ascribed to the availability of larvae was stronger. Thus, in the MIN system, the more prey. Also Altieri and Nicholls (2004) high- reduced abundance of new generation M. aeneus

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Vol.Vol. 1515 (2006):(2006): 61–72.1–000. and C. assimilis could have resulted from both the Goltermann, S. 1994. Das auftreten von laufkäfern (Col. lower number of rape flowers and the greater mor- Carabidae) auf winterrapsfeldern und deren einfluss auf den massenwechsel von Meligethes aeneus F. tality of pest larvae from the more abundant para- (Col. Nitulidae). PhD thesis, University of Rostock, sitoids and predators. Germany. Hokkanen, H. 1989. Biological and agrotehnical control of Acknowledgements. We thank Marge and Madis Ajaots, the rape blossom beetle Meligethes aeneus (Col., Nitid.). Acta Entomologica Fennica 53: 25–29. Pilsu Farm, for crop husbandry and two anonymous re- Hokkanen, H. & Holopainen, J.K. 1986. Carabid species viewers for constructive comments. This study was sup- and activity densities in biologically and conventionally ported by the EU Framework 5 project MASTER: Inte- managed cabbage fields. Journal of Applied Entomol- grated pest management strategies incorporating bio-con- ogy 52: 209–254. trol for European oilseed rape pests (QLK5-CT-2001- Irmler, U. 2003. The spatial and temporal pattern of carabid 01447) and Estonian Science Foundation grants Nr 5736 beetles on arable fields in northen Germany (Schles-(Schles- wig-Holstein) and their value as ecological indicators. and 4993. Rothamsted Research receives grant-aided sup- Agriculture, Ecosystems and Environment 98: 141– port from the UK Biotechnology and Biological Sciences 151. Research Council. 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. References Langmaack, M., Land, S. & Büchs, W. 2001. Effects of different field management systems on the carabid coe- Alford, D.V., Murchie, A.K. & Williams, I.H. 1995. Observa- nosis in oilseed rape with special respect to ecology tions on the impact of standard insecticide treatments and nutritional status of predacious Poecilus cupreus on Trichomalus perfectus, a parasitoid of seed weevil L. (Coleoptera, Carabidae). Journal of Applied Ento- on oilseed rape in the UK. Bulletin IOBC wprs 18, 4: mology 125: 313–320. 122–126. Lerin, J. 1987. A short bibliographical review of Trichomalus Alford, D.V., Nilsson, C. & Ulber, B. 2003. Insect pest of perfectus Walker, a parasite of the seed pod weevil oilseed rape crops. In: Alford, D.A. (ed.). Biocontrol of Ceutorhynchus assimilis Payk. Bulletin IOBC wprs 10: oilseed rape pests. Oxford, UK: Blackwell Science Ltd. 74–78. p. 10–41. Lewis, W.J., Stapel, J.O., Cortesero, A.M. & Takasu, K. Altieri, M.A. & Nicholls, C.I. 2004. Biodiversity and pest 1998. Understanding how parasitoids balance food and management in agroecosystems. 2nd ed. Food Prod- host needs: importance to biological control. Biological ucts Press. 236 p. Control 11: 175–183. Billqvist, A. & Ekbom, B. 2001a. Effects of host plant spe- Luik, A., Tarang, T. & Voolma, K. 2001. Carabids in refor refor-- cies on the interaction between the parasitic wasp estation areas and in the winter rape field of the forest Diospilus capito and pollen beetles (Meligethes spp.). neighbourhood. Journal of Forest Science 47: 123– Agricultural and Forest Entomology 3: 147–152. 126. Billqvist, A. & Ekbom, B. 2001b. The influence of host plant Meier, U. (ed.) 2001. Growth stages of mono- and dicotyle- species on the parasitism of pollen beetles (Meligethes donous plants. 2nd ed. Updated 00 Month Year. Cited spp.) by Phradis morionellus. Entomologia Experimen- 00 Month Year. Available on the Internet: http://www. talis et Applicata 98: 41–47. bba.de/veroeff/bbch/bbcheng.pdf Büch, R. 2002. Mortality of pollen beetle (Meligethes spp.) Metspalu, L. & Hiiesaar, K. 2002. Ristõieliste kultuuride kah- larvae due to predators and parasitoids in rape fields jurid. EPMÜ Taimekaitse Instituut, Tartu. p. 102. and the effect of conservation strips. Agriculture, Eco- Murchie, A.K. & Williams, I.H. 1998a. A bibliography of the systems and Environment 90: 225–263. cabbage seed weevil. Bulletin IOBC wprs 21: 163–169. Büchs, W. 2003a. Predators as biocontrol agents of oilseed Murchie, A.K. & Williams, I.H. 1998b. Effect of host size on rape pests. In: Alford, D.A. (ed.). Biocontrol of oilseed the sex of Trichomalus perfectus. Bulletin IOBC wprs rape pests. Oxford, UK: Blackwell Science Ltd. p. 279– 21: 177–181. 298. Murchie, A.K., Williams, I.H. & Alford, D.V. 1997. Effects of Büchs, W. 2003b. Impact of on-farm landscape structures commercial treatments to winter oilseed rape on para- and farming systems on predators. In: Alford, D.A. (ed.). sitism of Ceutorhynchus assimilis Paykull (Coleoptera: Biocontrol of oilseed rape pests. Oxford, UK: Blackwell Curculionidae) by Trichomalus perfectus (Walker) (Hy- Science Ltd. p. 245–227. menoptera: Pteromalidae). Crop Protection 16: 199– Büchs, W. & Nuss, H. 2000. First steps to assess the impor- 202. tance of epigaeic active polyphagous predators on Nilsson, C. 2003. Parasitoids of pollen beetles. In: Alford, oilseed rape insects pests with soil pupating larvae. D.A. (ed.). Biocontrol of oilseed rape pests. Oxford, UK: Bulletin IOBC wprs 23, 6: 151–163. Blackwell Science Ltd. p. 73–85.

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Pickett, J.A., Butt, T. M., Wallsgrove, R.M. & Williams, I.H. Management of oilseed rape pests. In: Alford, D.A. 1995. Minimising pesticide input in oilseed rape by ex- (ed.). Biocontrol of oilseed rape pests. Oxford, UK: ploiting natural regulatory processes. In: Proceedings Blackwell Science Ltd. p. 43–71. of the 9th International Rapeseed Congress. Cam- Williams, I.H. 2003. Parasitoids of cabbage seed weevil. In: bridge. p. 565–571. Alford, D.A. (ed.). Biocontrol of oilseed rape pests. Ox- Statistics Board 2003. Add the title of the statistics. Updated ford, UK: Blackwell Science Ltd. p. 97–112. 22 July 2005. Cited 20 October 2005. Available on the Williams, I.H. 2004. Advances in insect pest management Internet: http://pub.stat.ee/px-web.2001/Database/Ma- of oilseed rape in Europe. In Horowitz, A.R. & Ishaaya, jandus/Majandus.asp. I. (eds.). Insect pest management – ﬁeld and protected Thiele, H.-V. 1977. Carabid beetles in their enviroments. crops. Springer-Verlag: Heidelberg. p. 181–208. Zoophysiology and ecology 10. A study on habitat se- Williams, I.H., Büchs, W. Hokkanen, H., Johnen, A., Klu- lection by adaptations in physiology and behaviour. kowski, Z., Luik, A., Nilsson, C. & Ulber, B. 2002. MAS- Springer-Verlag, Berlin, Heidelberg, New York. 160 p. TER: management strategies for European rape pests Tryapitzyn, V.A. (ed.). 1978. Keys to the insect of the Euro-Euro- – a new EU Project. In: The BCPC Conference 18–21 pean part of the USSR, Volume III, Hymenoptera, Part November 2002. Conference Proceedings Vol. 2, II. Nauka: 758. (in Russian). Brighton, UK. p. 641–646. Tuubel, E. & Toom, T. 1999. The inﬂuence of pesticides on Williams, I.H. & Murchie, A.K. 1995. The role of parasitoids. arthropod predators fauna. Transactions of the Estoni- Agronomist, Spring 1995. p. 13–15. an Agricultural University 203: 180–183. Vinson, S.B. 1976. Host selection by insect parasitoids. An- Walters K.F.A., Young, J.E.B., Kromp, B. & Cox, P.D. 2003. nual Review of Entomology 21: 109–133.

7212 58 III 60 Integrated Control in Oilseed Crops IOBC/wprs Bulletin Vol. 29(7) 2006 pp. 165-172

Oilseed rape pests and their parasitoids in Estonia

Eve Veromann, Anne Luik and Reelika Kevväi Department of Plant Protection, Estonian Agriculture University, 64 Kreutzwaldi St. 51014, Tartu, Estonia

Abstract: The pests and their hymenopterous parasitoids present in spring and winter oilseed rape crop in Estonia were studied. Meligethes aeneus was abundant pest in the spring oilseed rape whereas Ceutorhynchus assimilis was more numerous in the winter oilseed rape. Other crucifer-specialist pests such as Ceutorhynchus sulcicollis, C. pallidactylus, C. rapae, C. floralis and C. pleurostigma were found but their abundance was very low. Also three parasitoids of M. aeneus larvae (Diospilus capito, Phradis morionellus and P. interstitialis) and three of C. assimilis larvae (Mesopolobus morys, Stenomalina gracilis and Trichomalus perfectus) were found. Larval parasitization rate of M. aeneus (0–7.4%) and C. assimilis (0–32%) was dependent on oilseed rape crop type and use of insecticides.

Key words: Oilseed rape, Meligethes aeneus, Ceutorhynchus assimilis, hymenopterous parasitoids.

Introduction

In Estonia, the cultivation of oilseed rape (Brassica napus L. and Brassica rapa L.) has expanded greatly in recent years and exceeded 50,400 ha in 2004 (Statistics Board, 2005). This provides a good substrate for population growth of crucifer-specialist, phytophagous pests. In Europe, the most common pests of oilseed rape are Meligethes aeneus Fabr., M. viridescens Fabr., Ceutorhynchus assimilis Payk., Ceutorhynchus pallidactylus Panz., C. napi Gylh., Dasineura brassicae Winn., Psylliodes chrysocephala L. and Phyllotreta nemorum, P. undulata and P. diademata (Alford et al., 2003). The management of pests on the European oilseed rape crop still relies heavily on chemical pesticides, most often applied routinely and prophylactically, without regard to pest incidence (Williams, 2004). This leads to the over-use of chemical pesticides, which reduces the economic competitiveness of the crop and threatens biological diversity. Pesticides also kill natural agents of biological control that represent a resource with a great potential benefit to farmers and consumers (Alford et al., 1995; Williams & Murchie, 1995). By killing the natural enemies of pests, pesticide use has to be increased further to achieve pest control (Pickett et al., 1995; Murchie et al., 1997). More than 30 species of hymenopterous parasitoids have been reported to attack C. assimilis in Europe (Williams, 2003) that can provide natural control of these pests. Of these, the larval ectoparasitoid Trichomalus perfectus Walker (Hymenoptera: Pteromalidae) is widely distributed and particularly important (Lerin, 1987; Murchie & Williams, 1998a). In addition to killing larvae through direct parasitism, it further reduces damage to infested pods by preventing host larvae from eating their full complement of seeds (Murchie & Williams, 1998b). Recent advances in insect management of the pests of oilseed rape have emphasised the important role of natural enemies within integrated pest management systems for the crop (Williams, 2004). The EU-funded project MASTER: MAnagement STrategies for European Rape pests aims to develop economically-viable and environmentally-acceptable crop management strategies for winter oilseed rape which maximise the biocontrol of key pests and minimise chemical inputs (Williams et al., 2002). This requires a much better under-

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standing of pest and parasitoid taxonomy and biology throughout Europe. The pests of oilseed rape and their natural enemies have been little studied in Estonia. The present study aims to add to the understanding of rape pests and their natural enemies in Estonia and contributes to the project MASTER. In Estonian conditions the cropping of spring oilseed rape is still prevailing but growing of winter oilseed rape is also increasing. The aim of this study was to identify key pests and their parasitoids on both winter and spring oilseed rape in Estonia and to compare the species composition on the two crops. Also, we determined the impact of insecticide use on the occurrence and phenology of oilseed rape pests and their hymenopteran parasitoids.

Materials and methods

A study with the winter oilseed rape (WOSR) cultivar ‘Banjo’, sown in August 2004 and the spring oilseed rape (SOSR) ‘Mozart’, sown in May 2005, was carried out on Pilsu Farm, Tartu County, Estonia (58°14´ latitude 26°16´ longitude). Both crops were grown with no insecticide (i0) and with insecticide (ii) cropping systems. The study site included two adjacent, approximately rectangular, 1 ha fields (two replicates for both crops). In the ii- system, the insecticide Fastac was used at green bud stage (BBCH growth stage (GS) 51 of Lancashire et al.,1991) and Karate was used at the end of flowering of the main raceme of oilseed rape plants (GS 67). Insects were sampled with yellow water traps (210 x 310 x 90 mm). Six traps per plot were positioned at the top of the crop canopy. Traps were emptied weekly from the beginning of flowering to pre-harvest of plants (GS 80). The growth stages of the rape plants were recorded weekly (Lancashire et al., 1991; see also Meier, 2001). Traps were put out on the winter oilseed rape field on 12 May (GS 52, inflorescence emergence stage of plants) until 28 June (GS 80; pod maturation stage) and on the spring oilseed rape fields on 15 June (GS 50, green bud stage) until 10 August (GS 80). In the laboratory, the insect samples were sorted and target cruciferous specialists and their key parasitoids were identified to species and counted. For estimation of parasitization levels, M. aeneus larvae were collected from oilseed rape flowers from 25 randomly chosen plants at each plot. Larvae were dissected in the laboratory. For the establishment of damage and parasitization assessments of C. assimilis, 25 plants were selected from each plot and all their pods were collected and incubated in emergence traps in laboratory conditions. Emerging parasitoids and larvae were counted and the percentage of damaged pods calculated. Statistical analysis was carried out using the SAS GENMOD procedure. The weekly target of pests and parasitoids were analysed applying the Poisson distribution and the log link function. For the repeated measures the generalized estimation equation analysis was used. The scale parameter was estimated by Pearson’s chi-square divided by the degrees of freedom if the model was overdispersed.

Results and discussion

During the study, 84 samples of WOSR and 192 of SOSR with a total of 12,918 specimens of crucifer-specialist insect pests from eight taxa were collected from the water traps (Figure 1). A more abundant crucifer-specialist community was found in the spring oilseed rape (11,177 specimens) than in the winter oilseed rape (1,742 specimens). Among them were the three major European pests: M. aeneus, C. assimilis and C. pallidactylus. The latter was not numerous – only a few specimens were found in winter oilseed rape. Meligethes aeneus was

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by far the most numerous and the only one to reach true pest status. Meligethes aeneus emerges from hibernation sites at the beginning of May in Estonia. Therefore, in winter oilseed rape it was not very numerous, but it was very abundant in spring oilseed rape, accounting for 98.6% of the crucifer-specialist specimens caught. Ceutorhynchus assimilis constituted 0.9% from the total number of specialists in spring oilseed rape but 18.8% in the winter oilseed rape. A few M. viridescens were also caught; this species requires higher temperatures for oviposition and development compared to M. aeneus (Alford et al., 2003) and therefore it is not abundant in Estonia. In addition, Ceutorhynchus sulcicollis, C. rapae, C. floralis and C. pleurostigma were also captured but their abundance was low (Figure 1).

100000 WOSR 11025 SOSR 10000 1286 1000 317 105 83 100 29 21 9 12 10 12 10 6 2 1 0 1 1

s s s lli ens o ilis lus ali c ty i rapae im lor tigma aeneu esc ac f . id C. id C. M ir uros .v C.sulc C.ass e M C.pall C.pl

Figure 1. The species composition and the total number of crucifer-specialists caught in yellow water traps (12 per system) in winter (WOSR) and spring (SOSR) oilseed rape on Pilsu Farm, Tartu County, Estonia, in 2005.

Meligethes aeneus started to colonise the winter oilseed rape from GS 63 (30% of flowers are open) and its population peaked shortly after, on May 26 (Figure 2). In winter oilseed rape M. aeneus abundance was higher in the unsprayed field (i0) than in the sprayed- field (ii) throughout the study period (Figure 2; �² = 10.27, df = 1, P = 0.001;). Because of the late spring in 2005, M. aeneus oviposited in both spring and winter oilseed rape. On June 8 (GS 67–69) larvae were found and collected from flowers. Dissection of larvae showed that the parasitization rate of larvae was greater in the untreated field (8.7%) than in the sprayed field (4.8%). In an earlier study between 2002 - 2004, M. aeneus did not damage winter oilseed plants (Tarang, et al., 2004, Veromann, et al., 2004, 2005). In Estonia, M. aeneus mostly uses winter oilseed rape plants for maturation feeding and moves to the spring oilseed rape field for oviposition. The highest number of M. aeneus in the winter oilseed rape was at the beginning of colonisation in spring oilseed rape. In the spring oilseed rape field, the M. aeneus population was 6.4 times greater than in winter oilseed rape (�² = 337.87, df = 1, P < 0.001). Meligethes aeneus had two population peaks, on June 22 and August 3 in spring oilseed rape. The first peak coincided with green bud stage (GS 50) that is the most

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vulnerable period for plants. Green bud stage of oilseed rape plants is the most suitable period for egg laying for M. aeneus (Alford, 2003). The second peak occurred during pod maturation (GS 80) and indicated emergence of the new generation from the soil. During the first peak and until the second peak, M. aeneus abundance was greater in the untreated field than in the insecticide-treated field, but the difference was not statistically significant. No parasitization was found in larvae from the insecticide-treated field. In the unsprayed field, the parasitization level was 3.4%. At the second peak, M. aeneus (new generation) abundance was greater in the treated field than in the untreated field (Figure 2, Aug 3: �² = 4.28, df = 1, P = 0.039; Aug 10: �² =21.64, df = 1, P < 0.001), despite the application of insecticide. This difference may be explained by parasitiods, but the possibility requires additional research.

Meligethes aeneus Median; Box: 25%, 75%; Whisker: Min, Max * Log-decimal

1000 N=6 * *

100 * * * *

i0 July 6 July /65 Aug 3 /80 June 2 /66 June 8 /68 July 13 /67 July 20 /78 July 27 /79 Aug 10 /80 May May 19 /52 May 26 /63 ii June 15 /72 June 22 /78 June 28 /80 June 22 /50 June 28 /60 WOSR Date/GS SOSR Figure 2. Abundance of Meligethes aeneus per yellow water trap caught at different growth stages (GS) in no-insecticide (i0) (white bars) and with insecticide (ii) (shaded bars) cropping system fields of winter (WOSR) and spring (SOSR) oilseed rape fields on the Pilsu Farm, Tartu County, Estonia, in 2005 (* indicates significant difference between treatments).

Ceutorhynchus assimilis was more numerous in the winter than the spring oilseed rape (Figures 1 & 3; �² = 54.35, df = 1, P < 0.001). The first C. assimilis were found on May 26 (GS 63 – 30% of rape plants flowers were open) and their abundance increased at pod development stage (GS 72) which is the suitable time for egg laying. This peak during pod maturation (GS 79–80) probably related to a new generation. Insecticide treatment decreased C. assimilis damage. In winter oilseed rape, 4.5% pods were damaged in the treated field and 14.4% in the untreated field, but larval parasitization was higher in the treated (13.6%) than in the untreated field (7.2%). In the spring oilseed rape, 0.6% and 3.7% pods were damaged in

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sprayed fields and unsprayed fields, respectively. The level of larval parasitism was dependent on insecticide application. No parasitoids were found in larvae from the treated field but larval parasitization reached 32% in the unsprayed field. In spring oilseed rape, C. assimilis abundance was greater in the untreated than the treated field (Figure 3; �² = 4.86, df = 1, P = 0.027), but in both cropping systems the numbers were still lower than in the winter oilseed rape. We conclude that C. assimilis is phenologically better synchronised with the winter oilseed rape where reproduction mainly takes place.

Ceutorhynchus assimilis No Median; Box: 25%, 75%; Whisker: Min, Max 35 N=6 30

20 * 15

-5

i0 July 6 /65 Aug 3 /80 June 2 June /66 8 June /68 July 13 /67 July 20 /78 July 27 /79 Aug 10 /80 May 19 /52 May 26 /63 ii June 15 June /72 22 June /78 28 June /80 22 June /50 28 June /60 WOSR Date/GS SOSR Figure 3. Abundance of Ceutorhynchus assimilis per yellow water trap caught at different growth stages (GS) in no-insecticide (i0) (white bars) and with insecticide (ii) (shaded bars) cropping systems of winter (WOSR) and spring (SOSR) oilseed rape fields on the Pilsu Farm, Tartu County, Estonia, in 2005 (* indicates significant difference between treatments).

We have identified three parasitoids of M. aeneus: Diospilus capito, Phradis morionellus and P. interstitialis and three parasitoids of C. assimilis: Trichomalus perfectus, Mesopolobus morys and Stenomalina gracilis in our studies (Figure 4). These parasitoid species have been found over most of Europe, from southern Sweden to France (Nilsson, 2003) and D. capito and P. morionellus parasitoids of M. aeneus have also been found in Finland (Hokkanen, 1989). The numbers of parasitoids of M. aeneus were 9.7 times greater than C. assimilis parasitoids. Diospilus capito was the most abundant parasitoid in both crops, however the numbers in the spring oilseed rape crop were 1.3 times greater than in the winter oilseed rape (�² = 176.23, df = 1, P < 0.0001). Diospilus capito is multivoltine with two or three generations in northern Europe (Billquist & Ekbom 2001; Nilsson, 2003). As the population of multivotine parasitoids in winter rape has been reported as very low (Nilsson, 2003), the

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high numbers of D. capito in winter oilseed rape in our study was surprising. The other important M. aeneus parasitoids in Europe – P. morionellus and P. interstitialis, were more numerous in the winter crop. The abundance of C. assimilis parasitoids caught from the winter and spring oilseed rape was similar and relatively low. A total of 21 specimens of the C. assimilis larval ectoparasitoids: Mesopolobus morys, Stenomalina gracilis, Trichomalus perfectus, in the winter oilseed rape field and 28 specimens in the spring oilseed rape field were found. A total of only eight specimens of S. gracilis, 15 specimens of M. morys and 26 specimens of T. perfectus were found. Trichomalus perfectus is a univoltine ectoparasitoid whose abundance peaks 2-4 weeks after migration of C. assimilis into the crop. New- generation parasitoids mate on emergence and leave the crop shortly before harvest. Only females overwinter, possibly in evergreen foliage (Williams, 2003).

120,00 WOSR 100,00 SOSR 80,00 60,00 40,00 20,00 0,00

s s o is s it l lu orys p m racili rfectu ca g e s rstitia ionel p u te or s il u sp is in al io d is m D a d m r ra o h h Mesopolobus Stenomalina ch P P Tri

Figure 4. The species composition and the total number of key parasitoids of oilseed rape pests caught in yellow water traps (12 per system) in winter (WOSR) and spring (SOSR) oilseed rape on Pilsu Farm, Tartu County, Estonia, in 2005.

In the winter oilseed crop, the number of parasitoids started to increase at the pod development stage (GS 72) and peaked at the end of pod development (GS 78). Abundance of parasitoids in winter oilseed rape was greater in the unsprayed (i0) field than in the sprayed (ii) field (Figure 5; �² =10.08, df = 1, P = 0.002). In the spring oilseed rape field, parasitoids were most numerous during pod ripening (GS 79–80). During the population peaks of the parasitoids, the dominant species in both fields was D. capito and their abundance was greater in the unsprayed field than in the sprayed field (�² = 5.95, df = 1, P = 0.015). Parasitoid phenology was synchronised with that of their hosts. Peak abundance of D. capito coincided with peak abundance of M. aeneus (GS 80) in both fields, indicating that they probably emerged from host larvae in the oilseed rape. We conclude that two cruciferous specialists Ceutorhynchus assimilis and Meligethes aeneus have impact for oilseed rape production in Estonia. The population of C. assimilis was greatest in winter oilseed rape where reproduction mainly takes place and was influenced by the parasitoids T. perfectus, M. morys and S. gracilis. Larval parasitization rate of C. assimilis (0–32%) was dependent on use of insecticides. The M. aeneus population was phonologically

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better synchronised with spring oilseed rape, where numerous individuals of the new generation developed. Meligethes aeneus larval parasitoids Diospilus capito, Phradis morionellus and P. interstitialis influence the population whereas parasitization rate (0–7.4%) was dependent on insecticide treatments.

Median; Box: 25%-75%; Whisker: Min-Max 40

15 * *

-5 Aug3/80

Aug10/80 i0 June2/66 June8/68 June6/65 July13 /67 July20 /78 July27 /79 May19 /52 May26 /63 June15 /72 June22 /78 June28 /80 June22 /50 June28 /60 ii WOSR Date/GS SOSR

Figure 5. Abundance of key parasitoids per yellow water trap caught at different dates and growth stages (GS) in no-insecticide (i0) (white bars) and with insecticide (ii) (shaded bars) cropping systems of winter (WOSR) and spring (SOSR) oilseed rape on the Pilsu Farm, Tartu County, Estonia, in 2005 (* indicates significant difference between treatments).

Acknowledgements

We thank Marge and Madis Ajaots, Pilsu Farm, for crop husbandry. This study was supported by the EU Framework 5 project MASTER: Integrated pest management strategies incorporating bio-control for European oilseed rape pests (QLK5-CT-2001-01447), Ministry of Agriculture of Estonia and Estonian Science Foundation grants Nr 5736 and 4993.

References

Alford, D.V., Murchie, A.K. & Williams, I.H. 1995: Observations on the impact of standard insecticide treatments on Trichomalus perfectus, a parasitoid of seed weevil on oilseed rape in the UK. – IOBC/wprs Bulletin 18 (4): 122-126.

67 172

Alford, D.V., Nilsson, C. & Ulber, B. 2003: Insect Pest of Oilseed Rape Crops. – In: Alford, D.A. (ed.). Biocontrol of Oilseed Rape Pests, Blackwell Science Ltd, Oxford, UK: 10-41. Billqvist, A. & Ekbom, B. 2001: Effects of host plant species on the interaction between the parasitic wasp Diospilus capito and pollen beetles (Meligethes spp.). – Agricultural and Forest Entomology 3: 147-152. Hokkanen, H. 1989: Biological and agrotechnical control of the rape blossom beetle Meligethes aeneus (Col., Nitidulidae). – Acta Entomologica Fennica 53: 25-29. Lancashire, P.D., Bleiholder, H., Boom, T.van D., Langelüddeke, 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. Lerin, J. 1987: A short bibliographical review of Trichomalus perfectus Walker, a parasite of the seed pod weevil Ceutorhynchus assimilis Payk. – IOBC/wprs Bulletin 10: 74-78. Meier, U. (ed.) 2001: Growth stages of mono- and dicotyledonous plants. 2nd ed. – http:// www.bba.de/veroeff/bbch/bbcheng.pdf Murchie, A.K. & Williams, I.H. 1998a: A bibliography of the cabbage seed weevil. – IOBC/wprs Bulletin 21 (5): 163-169. Murchie, A.K. & Williams, I.H. 1998b: Effect of host size on the sex of Trichomalus perfectus. – IOBC/wprs Bulletin 21 (5): 177-181. Murchie, A.K., Williams, I.H. & Alford, D.V. 1997: Effects of commercial treatments to winter oilseed rape on parasitism of Ceutorhynchus assimilis Paykull (Coleoptera: Curculionidae) by Trichomalus perfectus (Walker) (Hymenoptera: Pteromalidae). – Crop Protection 16: 199-202. Nilsson, C. 2003: Parasitoids of pollen beetles. – In: Alford, D.A. (ed.). Biocontrol of Oilseed Rape Pests. Blackwell Science Ltd, Oxford, UK: 73-85. Pickett, J.A., Butt, T. M., Wallsgrove, R.M. & Williams, I.H. 1995: Minimising pesticide input in oilseed rape by exploiting natural regulatory processes. – Proceedings of the 9th International Rapeseed Congress, Cambridge, 4–7 July: 565-571. Statistics Board 2005: Cited 3 Oct. 2005. Updated 22 July 2005. – http://pub.stat.ee/pxweb.2001/Database/Majandus/13Pellumajandus/10Taimekasvatus/10 Taimekasvatus.asp Tarang, T., Veromann, E., Luik, A. & Williams, I. 2004: On the target entomofauna of an organic winter oilseed rape field in Estonia. – Latvijas Entomologs 41: 100-110 Veromann, E., Kevväi, R., Luik, A., Metspalu, L. & Tarang, T. 2005: Pollen beetles (Meli- gethes aeneus F) on winter and spring oilseed rape. – Agronomy 2005. Transactions of the Estonian Agricultural University. Veromann, E., Tarang, T., Luik, A. & Metspalu, L. 2004: Pests and their natural enemies in oilseed rape in Estonia. – Latvian Journal of Agronomy 7: 12–14. Williams, I.H. 2003: Parasitoids of cabbage seed weevil. – In: Alford, D.A. (ed.). Biocontrol of Oilseed Rape Pests. Blackwell Science Ltd, Oxford, UK: 97-112. Williams, I.H., Büchs, W. Hokkanen, H., Johnen, A., Klukowski, Z., Luik, A., Nilsson, C. & Ulber, B. 2002: MASTER: Management Strategies for European Rape pests – a new EU Project. – The BCPC Conference 18–21 November 2002, Conference Proceedings, Brighton, UK 2: 641-646. Williams, I.H. 2004: Advances in insect pest management of oilseed rape in Europe. – In A.R. Horowitz & I. Ishaaya (eds.): Insect Pest Management – Field and Protected Crops. Springer-Verlag, Heidelberg: 181-208. Williams, I.H. & Murchie, A.K. 1995: The role of parasitoids. – Agronomist, Spring 1995: 13-15.

68 IV 70 – International Journal of Pest Management, 2007, in press.

Do cropping system and insecticide use in spring oilseed rape affect the abundance of pollen beetles (Meligethes aeneus Fab.) on the crop?

EVE VEROMANN1, REELIKA KEVVÄI1, ANNE LUIK1 & INGRID H. WILLIAMS2

1Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences; Kreutzwaldi 64, Tartu 51014, Estonia & 2Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK

Short title: Impact of cropping system

Abstract. The impact of minimised (MIN – no plough, direct drilling, no pesticides) and standard (STN – plough, standard application of pesticides) cropping systems on the abundance of old and new generations of Meligethes aeneus (Fabricius) (Nitiduli- dae, Coleoptera) was assessed in spring oilseed rape in 2003–2005 in Estonia. Old generation (previously overwintered) M. aeneus were more abundant in STN than in MIN crops, despite the application of insecticide, probably because the latter reduced M. aeneus damage to the buds, making STN crops more attractive to M. aeneus seeking feeding and oviposition resources. The abundance of new generation M. aeneus showed a strong linear increase over the three years, on both MIN and STN systems. In 2005, the abundance of new generation M. aeneus was signiﬁcantly greater in the STN than in the MIN ﬁeld. The study showed that the application of insecticides promotes population increase in new generation M. aeneus.

Keywords: Meligethes aeneus, spring oilseed rape, minimised and standard cropping system.

Correspondence: Eve Veromann, Institute of Agricultural and Environmental Sciences, Esto- nian University of Life Sciences; Kreutzwaldi 64, Tartu 51014, Estonia. Phone: +37255600901. Email: [email protected]

Introduction

In Estonia, cultivation of oilseed rape (Brassica napus L., Brassica rapa L.) has been prac- tised for only short time. The broader cultivation of this industrially important crop began only in the early nineties but has increased ten-fold over the past decade, reach- ing 50, 400 hectares in 2004 (Statistics Board 2006). This rapid increase in hectares has provided good potential for population growth of oilseed rape pests. Many different insect pests attack oilseed rape, but the pollen beetle, Meligeth- es aeneus Fab. (Coleoptera, Nitidulidae) is the most widespread pest throughout Europe in both winter and spring oilseed rape. It is usually more abundant in the spring crop (Alford et al. 2003). Meligethes aeneus is univoltine, migrating to the crop from overwintering sites in the spring (old generation). The adults feed on pollen in the buds and ﬂowers and the females lay their eggs in the buds. The new generation larvae feed on

71 pollen in the ﬂowers. Development from egg to larval maturity takes about four weeks. When mature, the larvae drop to the soil beneath the ﬂowering canopy to pupate. New generation adults emerge about two weeks later (Hokkanen 2000) and, after a short period of feeding, seek overwintering sites. In Estonia, M. aeneus is the most abundant crucifer-specialist insect and the only one to reach pest status in spring oilseed rape (Veromann et al. 2006a, b). The management of oilseed rape pests relies on chemical pesticides, often applied routinely without regard to pest incidence (Williams 2004). Pesticides sometimes also kill the natural enemies of the pest, which could control the pest (Nilsson 2003). Thus, in Estonia, we had the opportunity to determine how quickly the pest can build up its population and if the cropping system has an impact on the development of this population. The aim of this study was to compare the impact of reduced input (no plough, direct drilling, no pesticides) and conventional (plough, standard application of pesticides) cropping systems on the abundance of new generation of M. aeneus.

Materials and methods

The study compared a reduced input, referred to here as minimised (MIN), and a standard (STN) cropping system for spring oilseed rape in 2003–2005. The study site comprised two adjacent, approximately rectangular, fields (both 2 ha) on Pilsu Farm, Tartu County, Estonia (58°14´ latitude 26°16´ longitude in 2003 and 2004; 58°13´ latitude 26°11´ longitude in 2005). The soil was loamy with average KCI 6.15. The spring oilseed rape cultivar ‘Quantum’ (seeding rate 6 kg/ha) was drilled in all fields, following winter wheat in 2003 and 2005 and winter oilseed rape in 2004. In the STN system, soil preparation was by ploughing and pesticides were applied, whereas in the MIN system, direct drilling replaced ploughing (except in 2005, when both fields were ploughed) and no pesticides were applied (Table 1). The growth stages of the crops were recorded weekly (Lancashire et al. 1991, see also Meier 2001).

Table 1.

Insects were sampled with rectangular yellow water traps (210 x 310 x 90 mm deep), each containing about 1.5 litres of water, positioned at the top of the crop canopy. In 2003 and 2004, there were four traps, and in 2005, six traps per plot. Traps were placed out when plants were at the green bud stage (BBCH 50) and emptied weekly until just before harvest (BBCH 83). Insect samples were sorted in the laboratory and M. aeneus identified and counted. Those captured between BBCH 50–66 (bud and flowering stages) were recorded as the old overwintered generation, while those from BBCH 73 (30% of pods full size) and six weeks after first catch of the old generation, until BBCH 83 (30% of pods ripe, seeds dark and hard) were recorded as the new generation. Statistical analysis was carried out using the SAS GENMOD procedure. The old and new generations of M. aeneus were analysed applying the Poisson distribution and the log link function. For the repeated measures Wald Statistics for type 3 the generalized estimation equation analysis was used.

72 Results

Populations of both old and new generations of M. aeneus in both MIN and STN systems showed a general increase in size from 2003 to 2005 (Figure 1); this was particularly marked in the STN system where the increase was 5-fold. The old generation population was smallest in the MIN field in 2003, significantly smaller than that in all other fields except in the MIN field in 2004 (Table II). In each year, the old generation population was greater in the STN than in the MIN field, but the difference was statistically significant only in 2003 (χ=10.98; df=1; P<0.001). In both MIN and STN fields, the old generation population was greatest in 2005, and differed significantly from that in all other years.

Figure 1. Table 2.

As with the old generation, the size of the new generation population to emerge from the soil was smallest in the MIN field in 2003, significantly smaller than that in all other fields in 2004 and 2005 (Table 2). The new generation population size was greater in STN than in MIN fields, with differences significant in 2003 (χ=5.87; df=1; P=0.015) and in 2005 (χ=7.55; df=1; P=0.006). The new generation population size was greatest in the STN field of 2005, with differences compared with both other years and treatments highly significant (Table 2). In both MIN and STN systems, the new generation population size in 2004 and 2005 was significantly greater than in the previous year.

Discussion

In each of the three years and despite the application of insecticide to the STN fields, the old generation of M. aeneus was more abundant in the STN than in the MIN fields. Overwintered M. aeneus adults colonized both cropping system fields at the same time and in similar numbers. However treatment of the STN fields with insecticide reduced the numbers of M. aeneus at the vulnerable green bud stage of the crop. This in turn reduced damage to the buds and enabled the plants in the STN fields to produce noticeably more flowers than those in the MIN fields. STN fields treated with insecticide consequently offered more buds and flowers suitable for feeding and egg laying than MIN fields not treated with insecticide, and, for that reason, were more attractive to the old generation of M. aeneus than the MIN fields. Albeit in 2004 spring oilseed rape followed winter rape, the old generation of summer 2004 was of a similar size in the MIN field and even smaller in the STN field than in 2003. Thus, the long, cold winter of 2003/4 probably killed many hibernating M. aeneus. As in Finland (Hokkanen 1993, 2000), overwintering mortality could be a main factor determining population size. Nevertheless, the population of M. aeneus has a great tendency to grow, because the abundance of the old generation of M. aeneus in both fields in 2005 was significantly greater than in 2003.

73 The new generation M. aeneus showed a strong linear increase in population size over the three years, being always greater in fields with insecticide treatment. Ac- cording to Hokkanen (2000, Fig. 4), insecticide treatment at or above the threshold level will not significantly reduce the size of the new generation, because the maximum number of new generation adults emerge from the soil from much lower old generation beetle densities. Spraying helps to protect the crop yield of one season only. Our study showed that treatment of the old generation with insecticides increased the size of the new generation as the number of emerged beetles was always greater in STN than in MIN fields. Application of insecticide may thus not only result in more buds and flowers for feeding and egg-laying by M. aeneus but probably also kills its natural enemies, which have potential to decrease the size of the new generation of M. aeneus. Insecticides are known to kill both parasitoids (Hokkanen et al. 1988, Hokkanen 1989, Hokkanen 2006, Nilsson 2003, Williams 2004) and predators (Büchs 2003, Büchs et al. 2006, Hokkanen & Holopainen 1986, Veromann et al. 2006 b, Williams 2004) of M. aeneus. Luik et al. (2006) found that the number of parasitoids of M. aeneus and the population size and species diversity of predators was greater in fields with MIN than in those with STN cropping systems. Further, in the STN system, ploughing probably reduced parasitoid survival and diminished predator species diversity and abundance, whereas MIN cultivation was less destructive as found by Büchs 2003, Nilsson 1985, Nilsson et al. 2006 and Williams 2004. From our study we conclude that the STN cropping system promotes the increase of the population of M. aeneus.

Acknowledgements

We thank Marge and Madis Ajaots, Pilsu Farm, for crop husbandry. This study was supported by the EU Framework 5 project MASTER: Integrated pest management strategies incorporating bio-control for European oilseed rape pests (QLK5-CT-2001- 01447) and Estonian Science Foundation grants Nr 5736 and 4993. Rothamsted Re- search receives grant-aided support from the UK Biotechnology and Biological Sci- ences Research Council.

References

Alford DV, Nilsson C, Ulber B. 2003. Insect Pests of Oilseed Rape Crops. In: Alford DV, editor. Biocontrol of Oilseed Rape Pests. Blackwell Science Ltd, Ox- ford, UK, p 10–41. Büchs W. 2003. Impact of On-Farm Landscape Structures and Farming Systems on Predators. In: Alford DV, editor. Biocontrol of Oilseed Rape Pests. Black- well Science Ltd, Oxford, UK, p 245–227. Büchs W, Felsmann DS, Klukowski Z, Luik A, Nilsson C, Ahmed B, Ulber B, Williams IH. 2006. Key predator species in oilseed rape crops – a review of literature and MASTER results. CD-ROM Proceedings of International symposium on integrated pest management in oilseed rape, 3–5 April, 2006, Göttingen, Germany.

74 Hokkanen H. 1989. Biological and agrotehnical control of the rape blossom beetle Meligethes aeneus (Col. Nitid.). Acta Entomol. Fennica 53: 25–29. Hokkanen HMT. 1993. Overwintering survival and spring emergence in Meligethes aeneus: effects of body weight, crowding, and soil treatment with Beauveria bassiana. Entomol. Exp. Appl. 67: 241–246. Hokkanen HMT. 2000. The making of a pest: recruitment of Meligethes aeneus onto oilseed Brassicas. Entomol. Exp. Appl. 95: 141–249. Hokkanen HMT. 2006. Phradis morionellus on Meligethes aeneus: long term patterns of parasitism and impact on pollen beetles populations in Finland. CD-ROM Proceedings of International symposium on integrated pest management in oilseed rape, 3–5 April, 2006, Göttingen, Germany. Hokkanen H, Holopainen JK. 1986. Carabid species and activity densities in biologically and conventionally managed cabbage ﬁelds. J. Appl. Entomol. 52: 209–254. Hokkanen H, Husberg GB, Söderblom M. 1988. Natural enemy conservation for the integrated control of the rape blossom beetle Meligethes aeneus F. Ann Agr. Fenn. 27: 281–294. Lancashire PD, Bleiholder H, van Boom TD, Langelüddeke P, Strauss P, Weber E, Wit- zenberger A. 1991. A uniform decimal code for stages of crops and weeds. Ann. of Appl. Biol. 119: 561–601. Luik A, Veromann E, Kevväi R, Kruus M. 2006. A comparison of the pests, parasitoids and predators on winter and spring oilseed rape crops in Estonia. CD-ROM Proceedings International symposium on integrated pest management in oilseed rape, 3–5 April, 2006, Göttingen, Germany. Meier U, editor. 2001. Growth stages of mono- and dicotyledonous plants. 2nd ed. Updated 23 November 2005. [Cited 12 April 2006] Available from: http://www.bba.de/veroeff/bbch/bbcheng.pdf Nilsson C. 1985. Impact of ploughing on emergence of pollen beetle parasitoids after hibernation. J. Appl. Entomol. 100: 302–308. Nilsson C. 2003. Parasitoids of Pollen Beetles. In: Alford DV, editor. Biocontrol of Oilseed Rape Pests. Blackwell Science Ltd, Oxford, UK, p 73–85. Nilsson C, Ulber B, Williams IH, Ferguson AW. 2006. Effects of post-harvest soil tillage on the survival of key parasitoids of oilseed rape pests. CD-ROM Proceedings International symposium on integrated pest management in oilseed rape, 3–5 April, 2006, Göttingen, Germany. Statistics Board [Internet] 2005 [cited 10 October 2006]; Updated 31 July 2006; Avail- able on: http://pub.stat.ee/px-web.2001/ Veromann E, Luik A, Metspalu L, Williams IH. 2006a. Key pests and their parasitoids on spring and winter oilseed rape in Estonia. Entomol. Fennica 17: 400–404. Veromann E, Tarang T, Kevväi R, Luik A, Williams IH. 2006b. Insect pest and their natural enemies on spring oilseed rape in Estonia: impact of cropping systems. Agr. Food Sci. 15: 61–72. Williams IH. 2004. Advances in insect pest management of oilseed rape in Europe. In: Horowitz AR, Ishaaya I, editors. Insect pest management – ﬁeld and protected crops. Springer-Verlag, Heidelberg. p 181–208.

75 Figure legends

��

Figure 1. Mean abundance (± SD) of old and new generation of M. aeneus per trap on Pilsu Farm, Tartu County, 2003–2005.

Table 1. Dates of soil cultivation, sowing, fertilization and application of pesticides to spring oilseed rape ﬁelds on Pilsu Farm, Tartu County, 2003–2005.

STN MIN 2003 2004 2005 2003 2004 2005 Plough 28 Aug 7 Sept 26 Aug – – 26 Aug 2002 2003 2004 2004 Rolling – 1 May 27 April – 1 May 27 April Cultivation 11 May 5 May – – – – Herbicide 11 May, 5 May 9 May, – 5 May 9 May, 3 June 13 June 13 June Fertilizer 12 May 7 May 8 May, 12 May 7 May 8 May, 2 July 12 June, 21 2 July 12 June, June 21 June Seeding 12 May 7 May 10 May 12 May 7 May 10 May Fungicide 23 June – 4 July – – 4 July Insecticide 15 July 21 May, 21 June, – – – 22 June 4 July

76 - 2005 MIN 0,006 STN ns 0,01 2004 M. aeneus between treat MIN ns 0,013 0,0002 New Generation New STN ns 0,003 0,0001 0,0001 2003 MIN 0,015 0,0001 0,0001 0,0001 0,0001 2005 MIN ns STN 0,0001 0,0001 2004 MIN ns 0,0001 0,0001 Old generation Old STN 0,008 ns 0,013 0,002 2003 MIN 0,001 ns 0,0008 0,0001 0,0001 ments and years on Pilsu Farm, Tartu County, 2003–2005 (ns – not signiﬁcant). County, Tartu Farm, on Pilsu ments and years STN 2003 MIN 2004 STN 2004 MIN 2005 STN 2005 Table 2. Table differences (P<) Statistical of the abundance of old and new generations of

77 CURRICULUM VITAE

Eve Veromann

First name: Eve Surname: Veromann

Institution: Department of Plant Protection, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 64, Tartu, 51014, Estonia E-mail: [email protected]

Position: Technician Date of birth: 27 May 1961

Education: 1981–1986 University of Tartu, Faculty of Biology and Geography, Biology 1968–1979 Paide Secondary School No 3

Foreign languages: English, Russian

Professional employment: Since 2002 Institute of Agricultural and Environmental Sciences, technician Since 1993 Estonian Nature Photo, bookkeeper, editor 1986–1993 Institute of Zoology and Botany, engineer

Academic degree: Master’s degree, entomology. Thesis: Pests and their parasitoids in an organic winter oilseed rape. Site of receiving the degree: Estonian Agricultural University, 2003

Research-administrative experience: 2002–2006 Integrated pest management strategies incorporating bio-control for European oilseed rape pests QLK5-CT- 2001-01447, MASTER: MAnagement STrategies for European Rape pests.

78 Research interests: Investigation of hymenopteran parasitoids of oilseed rape pests, insect ecology, social insects.

Target financed (TF) projects and grants of the Estonian Science Foun- dation (ESF): 2006–2009 ESF grant No 6722: Delayed effects of sublethal doses of natural insecticides on pest and beneficial insects, PhD student. 2004–2008 TF project SF0172655s04: Development of environmentally-friendly plant protection II, PhD student. 2004–2007 ESF grant No 5736: Occurrence of carabids and hymenopterous parasitoids in different crops depending on growing technologies and field locations, PhD student. 2002–2005 ESF grant No 4993: The effectiveness of entomophags and entomopathogens in the natural control of pests in oilseed rape and cabbage fields depending on the type, variation and diversity of the surrounding vegetation of the crops in ecological and intensive cultivation conditions, PhD student.

Professional training: 2006 PhD course on Insect Pollinators and Pollination Ecology, Univer- sity of Helsinki, Finland. 2006 PhD course on Mathematical Statistics and Modelling, EMÜ, Esto- nia. 2006 PhD course on Methodology of Scientiﬁc Research, EMÜ, Estonia. 2005 PhD course on Academic Writing and Presentation, EMÜ, Esto- nia. 2004 PhD course on Social Insects, SLU, Sweden. 2003 to further the knowledge of Taxonomy of Hymenopteran Parasi- toids, Rothamsted Research, UK. 2002 course on The Taxonomy and Biology of Parasitic Hymenoptera, Natural History Museum & Imperial College, Silwood Park, UK. 2002 study of oilseed rape pests and their parasitoids, Rothamsted Re- search, UK.

79 CURRICULUM VITAE

Eve Veromann

Eesnimi: Eve Perekonnanimi: Veromann

Töökoht: Taimekaitse osakond, EMÜ põllumajandus- ja keskkonnainstituut, Kreutzwaldi 64, Tartu, 51014 E-mail: [email protected]

Ametikoht: Tehnik

Sünniaeg: 27. mai 1961

Haridus: 1981–1986 Tartu Riiklik Ülikool, Bioloogia ja Geograaﬁa teaduskond, bioloog 1968–1979 Paide III Keskkool

Võõrkeelte oskus: Inglise ja vene keel

Teenistuskäik: Alates 2002 EMÜ põllumajandus- ja keskkonnainstituut, tehnik Alates 1993 Eesti Loodusfoto OÜ, raamatupidaja, toimetaja 1986–1993 TA Zooloogia ja Botaanika Instituut, insener

Teaduskraad: Teadusmagister (MSc), väitekiri: Talirapsi kahjurid ja nende parasitoidid maheviljeluse tingimustes.

Teaduskraadi välja andnud asutus: EPMÜ, 2003

Teadusorganisatsiooniline tegevus: 2002–2006 Integreeritud tõrjestrateegiad kaasaarvatud bioloogiline tõrje Euroopa rapsikahjuritele QLK5-CT-2001-01447, MASTER: MAnagement STrategies for European Rape pests.

80 Uurimistöö põhisuunad: Rapsikahjurite ja nende kiletiivaliste parasitoidide liigilise koos- seisu väljaselgitamine ja nende arvukust mõjutavate tegurite uurimine, putukate ökoloogia ja sotsiaalsed putukad.

Projektid: 2006–2009 Eesti teadusfondi grant 6722: “Looduslike insektitsiidide subletaalsete dooside järeltoime kahjuritele ja kasuritele”, täitja. 2004–2008 Sihtﬁnantseeritav teema SF 0172655s04: “Keskkonna- säästliku taimekaitsetehnoloogia arendamine II”, täitja. 2004–2007 Eesti teadusfondi grant 5736: “Jooksiklaste ja kiletiivaliste parasitoidide esinemine erinevates kultuurides sõltuvalt kasvatustehnoloogiast ning põllu äärealadest”, täitja. 2002–2005 Eesti teadusfondi grant 4993: “Entomofaagide ja entomo- patogeenide efektiivsus kahjurite looduslikus tõrjes rapsi ja kapsa põldudel sõltuvalt kultuuride sordist, teisenditest ja ümbritseva taimkatte mitmekesisusest ökoloogilise ja intensiivviljeluste tingimustes”, täitja.

Erialane täiendamine: 2006 NOVA/BOVA kraadiõppurite kursus doktorantidele: “Putuktol- meldajad ja tolmeldamisökoloogia”, Helsingi Ülikool, Soome. 2006 kraadiõppurite kursus doktorantidele: “Matemaatiline statistika ja modelleerimine”, EMÜ, Eesti. 2006 kraadiõppurite kursus doktorantidele: “Teadustöö metodoloogia”, EMÜ, Eesti. 2005 kraadiõppurite kursus doktorantidele: “Akadeemiline kirjutamine ja esitlus”, EMÜ, Eesti. 2004 NOVA kraadiõppurite kursus doktorantidele: “Sotsiaalsed putukad”, SLU, Rootsi. 2003 täienduskursus: “Rapsikahjurite kiletiivaliste parasitoidide määra- mine ja võrdlemine kontroll-eksemplaridega”, Rothamsted’i Uuri- misinstituut, Inglismaa. 2002 täienduskursus: “Parasitoidsete kiletiivaliste taksonoomia ja bioloogia”, Natural History Museum & Imperial College, Inglismaa. 2002 täienduskursus: “Rapsikahjurite ja nende kiletiivaliste parasitoidide taksonoomia ja määramine”, Rothamsted’i Uurimisinstituut, Inglismaa.

81 LIST OF PUBLICATIONS

1.1. Publications indexed in the ISI Web of Science database:

Veromann, E., Kevväi, R., Luik, A. & Williams, I. H. 2007. Do cropping system and insecticide use in spring oilseed rape affect the abundance of pollen beetles (Meligethes aeneus Fab.) on the crop? International Journal of Pest Management, in press. Veromann, E., Luik, A., Metspalu, L., & Williams, I. 2006. Key pests and their parasitoids on spring and winter oilseed rape in Estonia. Entomologica Fennica 17, 400–404. Veromann, E., Tarang, T., Kevväi, R., Luik, A. & Williams, I. H. 2006. Insect pest and their natural enemies on spring oilseed rape in Es- tonia: impact of cropping systems. Agricultural and Food Science, 15, 61–72.

1.2. Papers published in other peer-reviewed international journals with a registered code:

Veromann, E., Luik, A. & Kevväi, R. 2006. The impact of ﬁeld edges on the incidence of Meligethes aeneus Fab. larvae and their parasitisation in spring and winter oilseed rape. Agronomy Research, 4, 447–450. Kevväi, R., Veromann, E. & Luik, A. 2006. Cabbage seed weevil (Ceu- torhynchus assimilis Payk.) and its parasitoids in oilseed rape crops in Estonia. Agronomy Research, 4, 227–230. Veromann, E., Tarang, T., Luik, A. & Metspalu, L. 2004. Pests and their natural enemies in oilseed rape in Estonia. Latvian Journal of Agronomy, 7, 12–14. Tarang, T., Veromann, E., Luik, A. & Williams, I. H. 2004. On the target entomofauna of an organic winter oilseed rape ﬁeld in Estonia”. Latvias Entomolgs, 41, 100–110.

82 3.4. Papers published in the proceedings of international conferences:

Veromann, E., Luik, A. & Kevväi, R. 2006. Dynamics of parasitoids in oilseed rape crops in Estonia. Proceedings of International Sympo- sium of Integrated Pest Management in Oilseed Rape, Göttingen, 3–5 April 2006. Veromann, E., Luik, A. & Kevväi, R. 2006. Impact of nematode Stein- ernema feltiae on the abundance of a new generation of pollen beetle (Meligethes aeneus Fab.) and its larval endoparasitoid Diospilus capito Nees in a spring oilseed rape ﬁeld in Estonia. Proceedings of International Conference of Information Systems in Sustain- able Agriculture, Agroenvironment and Food Technology, Volos, Greece, 20–23 September, 363–366. Veromann, E., Luik, A. & Kevväi, R. 2006. Oilseed rape pests and their parasitoids in Estonia. Bulletin IOBC/wprs, Integrated Control in Oilseed Crops, 29, 165–172. Luik, A., Veromann, E., Kevväi, R. & Kruus, M. 2006. A comparison of the pests, parasitoids and predators on winter and spring oilseed rape crops in Estonia. Proceedings of International Symposium of Integrated Pest Management in Oilseed Rape, Göttingen, 3–5 April 2006. Ulber, B., Fischer, K., Klukowski, Z., Luik, A., Veromann, E., Nilsson, C., Ahman, B., Williams, I. H., Ferguson, A. & Barari, H. 2006. Identity and potential of parasitoids for oilseed rape pests in Eu- rope. Proceedings of International Symposium of Integrated Pest Management in Oilseed Rape, Göttingen, 3–5 April 2006. Luik, A., Hanni, L., Merivee, E., Ploomi, A., Tarang, T. & Veromann, E. 2005. Studies in environmentally friendly plant protection in Estonia. NJF-Seminar 369, Organic farming for a new millennuim – status and future challenges. 15–17 June, SLU, Alnap, Sweden, NJF Report, 1 (1), 173–175. Veromann, E., Luik, A., Kevväi, R., Tarang, T. & Kruus, M. 2005. Pests and their natural enemies in the organic oilseed and turnip rape. NJF seminar no. 369, Organic farming for a new millennuim – status and future challenges. 15–17 June, SLU, Alnap, Sweden, NJF Report, 1 (1), 99–102. Luik, A., Tarang, T., Veromann, E., Kikas, A. & Hanni, L. 2002. Cara- bids in the Estonian crops. Proceedings International Conference of Plant Protection in the Baltic Region in the Context of the Integra- tion to the EU, Kaunas, Lithuania, 26–7 September, 68–71.

83 3.4. Papers published in the proceedings of Estonian conferences:

Veromann, E. & Luik, A. 2006. Agrotehnoloogilised võtted naeri-hiilamardika (Meligethes aeneus Fab) arvukuse looduslikuks regulatsioo- niks. Agronoomia 2006, 236–239. Veromann, E., Kevväi, R., Luik, A., Metspalu, L. & Tarang, T. 2005. Naeri- hiilamardikas (Meligethes aeneus F.) tali- ja suvirapsil. Agro- noomia 2005, 204–206. Kevväi, R., Veromann, E. & Luik, A. 2005. Naeri- hiilamardikas (Meli- gethes aeneus F.) ja tema parasitoidid suvirapsil. Agronoomia 2005, 207–209. Veromann, E. 2003. Talirapsi kahjurid ja nende parasitoidid maheviljeluse tingimustes. Magistritöö entomoloogia erialal. Eesti Põllu- majandusülikool, Agronoomia teaduskond, Taimekaitse instituut, Tartu, 56 lk. Veromann, E., Luik, A. & Metspalu, L. 2002. Talirapsi kahjurite parasitoidid mahepõllul. EPMÜ Agronoomiateaduskond. Teesid, Teadus- lik-praktiline konverents, 28. nov. 2002.

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