Proceedings of the Meetings Comptes Redus de les Réunions

IOBC / WPRS Working Group Integrated Protection in Field Vegetable Crops OILB / SROP Groupe de Travail «Lutte Intégrée en Culture de Légumes» Proceedings of the Meetings Comptes Redus de les Réunions at / à Gödöllö (Hungary) 31.10. 3.11.1999 and Krakow (Poland) 15. 17.10.2001 Edited by Stefan Vidal IOBC wprs Bulletin Bulletin OILB srop Vol. 26 (3), 2003

The content of the contributions is in the responsibility of the authors The IOBC/WPRS Bulletin is published by the International Organization for Biological and Integrated Control of Noxious Animals and Plants, West Palearctic Regional Section (IOBC/WPRS) Le Bulletin OILB/SROP est publié par l Organisation Internationale de Lutte Biologique et Intégrée contre les Animaux et les Plantes Nuisibles, section Regionale Ouest Paléarctique (OILB/SROP) Copyright: IOBC/WPRS 2003 The Publication Commission of the IOBC/WPRS: Horst Bathon Federal Biological Research Center for Agriculture and Forestry (BBA) Institute for Biological Control Heinrichstr. 243 D-64287 Darmstadt (Germany) Tel +49 6151 407-225, Fax +49 6151 407-290 e-mail: h.bathon.@bba.de Luc Tirry University of Gent Laboratory of Agrozoology Department of Crop Protection Coupure Links 653 B-9000 Gent (Belgium) Tel +32-9-2646152, Fax +32-9-2646239 e-mail: luc.tirry@ rug.ac.be Address General Secretariat: INRA Centre de Recherches de Dijon Laboratoire de recherches sur la Flore Pathogène dans le Sol 17, Rue Sully, BV 1540 21034 DIJON CEDEX France ISBN 92-9067-151-1 Web: http://www.iobc-wprs.org

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 307-314 Effects of flowering field margins on flight activity of the diamondback moth (Plutella xylostella L.) and its parasitoids Diadegma spp., and observations on distance from field edge, and vertical position of traps T. Bukovinszky 1, M.J. Brewer 2, K. Winkler 1, H. Trefas 1,3, L.E.M. Vet 1,4 & J.C. van Lenteren 1 1 Wageningen University and Research Centre, Laboratory of Entomology, Wageningen 6700 EH, The Netherlands. 2 University of Wyoming, Renewable Resources-Entomology 3 Szent István University, Department of Crop Protection, Gödöllõ, Hungary 4 Netherlands Institute of Ecology, Centre for Terrestrial Ecology, Heteren, The Netherlands Abstract: We studied the effects of flowering field margins on flight activity of the diamondback moth (Plutella xylostella L.) and its parasitoids Diadegma spp. in Brussels sprout fields (Brassica oleracea cv gemmifera var. Icarus), twice during the summer of 2000. We also compared the effect of vertical position of traps on insect counts, to investigate movement of insects within the field margin and field. Diamondback moth adults were attracted to flowering field margins. There was an increase in moth counts with increasing distance from the field edge. Flowers adjacent to the field influenced this pattern in the second observation period; as overall density of the moths inside the field was higher when flowering margins were present. Traps at higher position within the margin (level of flowers), caught more moths, than traps at lower position, whereas within-field field catches were higher in traps placed lower (canopy of plants) than in traps just above the canopy. However, this tendency changed to the opposite in the second observation period. Spatial patterns in catches of Diadegma spp. were in general similar to those of the diamondback moth. Although there was an increase in counts with increasing distance from the field edge, parasitoid counts over distance were not significantly influenced by the flowering field margin. Within the fields, traps at a lower position caught consistently more individuals then traps at a higher position. This finding suggests that this species is indeed a specialist in cruciferous habitats and its flight activity within the crop is restricted to the plant canopy. Results show that flowering field margins may act as trap crops by attracting populations of specialist herbivores, a reason to this might have been the high abundance of Sinapis alba in the margin. Field margins also increased pest densities in adjacent fields. Vertical position of traps affects efficiency of catches, and may influence the reliability of detection and estimation of herbivore and parasitoid populations. Keywords: Plutella xylostella, Diadegma spp., Sinapis alba, flowering field margin, habitat manipulation Introduction Diamondback moth Plutella xylostella (L.) is the most important insect pest of cruciferous crops throughout the world (Talekar and Shelton, 1993). The costs of chemical control and the increasing resistance against pesticides urges the development of alternative control methods against this pest (Charleston and Kfir, 2001). Diadegma semiclausum (Hellén) and 307

308 Diadegma fenestrale (Holmgren) (Hymenoptera: Ichneumonidae) are two of its few parasitoids and can be major mortality factors of the diamondback moth (Waage, 1983). However, their efficiency is often low in newly planted cruciferous habitats, because their host is often better able to establish itself (Talekar and Shelton, 1993). The goal of habitat management is to create a suitable infrastructure within the agricultural landscape by selectively providing resources for beneficial natural enemies to enhance natural control of pests (conservation biological control). A way to provide pollen/nectar sources for parasitoids, is to establish flowering field margins. Such margins may accumulate natural enemies of pests and increase their efficiency as control agents in adjacent fields. However, when herbivores can make use of them, field margins may also increase pest problems (Landis et al., 2000), raising interest in composing field margins selectively for pest control (Baggen et al., 1999). As cyclic colonisation of annual agroecosystems by herbivores and their parasitoids is a scale dependent process, the spatial dynamics of pests and beneficials in and around fields is an important issue in the establishment of flowering field margins (Bowie et al. 1999). Our aim was to study the effects of flowering field margins on spatial distribution of the diamondback moth and its parasitoids Diadegma spp. in Brussels sprout fields (Brassica oleracea cv gemmifera var. Icarus). We compared the effect of vertical position of traps on insect counts, to investigate where insect movement took place in the field margin and within the field. Materials and methods Experimental design Experiments were carried out on four Brussels sprout (Brassica oleracea var gemmifera cv. Maximus) plots (50mx80m) in the vicinity of Wageningen (The Netherlands) during the summer of 2000. The experimental site was located in a woodland area dominated by oak. Plots were isolated by a path of mown grass (mixture of Lolium spp. and Poa spp.) of at least 10m at each side. Flowering field margins (4mx50m) were established on the southwestern side of two of the plots in the direction of prevailing wind. Flowering field margins were composed of 27 plant species known to be used by insects as pollen and nectar source (Frei and Manhart, 1992, Table 1.). The time of flowering and percentage of cover by each plant species were monitored once a week in 10 randomly chosen square meters per flowering margin. Control plots were surrounded by mown grass on all sides. Sampling insect populations To monitor flight activity of the diamondback moth and its parasitoids Diadegma spp., we coated clear plastic circular traps (h=21cm, d=9cm) with transparent adhesive (Tanglefoot ), affixed them to a cane and placed them within the field margin and adjacent field. Traps were set to the height of the canopy of Brussels sprout plants (15cm above ground) and just above the canopy (50cm above ground) at four different distances from the field edge. The first trap line was placed within the field edge (0.75m from the border of the field), a second at 0.75m, a third at 6m, and a fourth line at 15m into the B. sprout field. Each trap line contained 3 traps of both vertical positions. We set the traps out in the field twice; in the periods of 5 th of July - 13 th of July (week 27-28) and 19 th of July 26 th of July (week 29-30). Traps were collected at the end of each sampling period, and were taken to the laboratory for identification of the specimens.

309 Data analysis Before the analysis, insect counts were value 1 transformed. A general linear model for analysis of variances was built to detect sources of significant variation between groups (SPSS 8.0). Each sampling period was analysed separately. Results and discussion During the observation period 5 to 11 plant species flowered in the field margins (Table 1), the dominant species were white mustard (Sinapis alba) and buckwheat (Fagopyrum esculentum). Table 1. The period of flowering and the percentage of cover of plant species recorded within the field margin during the summer season. X- indicates flowering Plant species % Week cover 27 28 29 30 Anthemis tinctoria 1 Arthemis arvensis 1 Borago officinalis 1 Capsella bursa-pastoris 1 X X X X Centaurea cyanus 2-5 Chenopodium album 5 Erodium cicutarium 1 X X X X Fagopyrum esculentum 10 X X X X Galeopsis sp. 1 X X X Galinsoga parviflora 1 Matricaria chamomilla 1 Matricaria inodora 1 Matricaria matricarioides 1 Medicago lupulina 1 Papaver rhoeas 1 Plantago lanceolata 1 X Plantago major 1 X X Polygonum persicaria 2-5 Sinapis alba 30 X X X X Solanum nigrum 1 X Sonchus arvensis 1 Spergula arvensis 1 X Stellaria media 1 X Trifolium incarnatum 2 Trifolium pratense 2 Veronica arvensis 1 X X X Viola arvensis 1 X X X X Diamondback moth adults were attracted to the flowering field margins (Table 2). Host plant allelochemicals are known to influence host location by the diamondback moth. The

310 olfactory attraction of the diamondback moth to volatiles from the white mustard (Brassica hirta) has been demonstrated earlier (Palaniswamy and Gillot, 1986). Table 2. Statistics (General Linear Model) on the effects of type of field margin, trap position, distance from edge of field and trap line on numbers of diamondback moth (Plutella xylostella L.) adults in the first (a) and second (b) sampling periods. Nonsignificant interactions are omitted from the model. a) Source of variation Type III SS df MS F P Field edge 6.22 1 6.22 4.72 0.0327 Position 52.99 1 52.99 40.24 <0.0001 Distance 30.81 3 10.27 7.79 0.0001 Trap Line 4.42 2 2.21 1.68 0.1932 Field edge x Distance 27.86 3 9.29 7.05 0.0003 Position x Distance 28.32 3 9.44 7.17 0.0003 Error 108.01 82 1.32 b) Source of variation Type III SS df MS F P Field edge 126.65 1 126.65 21.01 0.0002 Position 48.64 1 48.64 8.07 0.0056 Distance 178.83 3 59.61 9.89 <0.0001 Trap Line 5.29 2 2.65 0.44 0.6463 Field edge x Position 39.17 1 39.17 6.49 0.0126 Error 524.51 87 6.03 It is known to be attracted to, and sustain feeding and reproduction on Sinapis alba (Talekar and Shelton 1993). Although the flowering field margin might have acted as a trap crop in the field, it also increased overall density of the moths inside the field. Although catches inside the fields were not different between the treatments in the first sampling period (P=0.814; Fig.1.), the number of moths in fields with flowering margin was higher than in the control plots in the second sampling period (P=0.001; Fig. 2.). Trap line did not influence abundance of the diamondback moth, whereas distance of traps from the field edge had a significant spatial effect (Table 2a.b.) in both sampling periods. More moths were caught with increasing distance from the edge both in the treatment and the control plots (Fig. 1.). Distribution of moths over distance were different in the plots with flowering margin then in the ones without, as interaction term between the type of field margin and distance was significant (Table 2a., Fig. 1.), although this tendency was not present in the second sampling period. Within the flowering margins traps at higher position (at the level of flowers, Fig. 1a., 2a.), caught more moths, than traps at lower position (Fig 1b., 2b.), which may be explained both by oviposition preference within a plant and foraging for nectar sources. The accessibility of nectar from flowers of buckwheat as food source for diamondback moth adults has been demonstrated (Winkler in prep.). Within the field lower traps caught more moths in the first week than upper ones, but this tendency changed to the opposite in the second observation period (Table 2b.).

311 Fig. 1. Mean (± SE) number of diamondback moth caught in traps placed high (above) and low (below.) in Brussels sprout fields, at different distances from the border. Grey bars are fields with flowering margin, white bars are fields without flowers in the first sampling period. Most of the Diadegma spp. specimens caught belonged to D. semiclausum; the other, less abundant species found was D. fenestrale. Spatial patterns in catches of Diadegma spp. were similar to those of the diamondback moth (Fig.3a.b.). Within-field catches of Diadegma spp. were not different between the treatments in the first sampling period (P=0.307), but catches inside the fields with flowering margin were higher in the second sampling period (P<0.001). There was an increase in counts with increasing distance from the field edge (Table 3.). Trap line did not influence parasitoid distribution, but vertical position of traps did (Table 3.). Inside flowering margins traps at higher position (Fig. 3a.) caught more wasps, than traps at lower position (Fig 3b.). Specialist parasitoids may use infochemicals from the plant level to find their host (Vet and Dicke, 1992). Diadegma insulare prefers to search on wild cruciferous plant species over cultivated ones (Fox and Eisenbach, 1992). It is possible that Diadegma spp. were also attracted to field edges due to the presence of Sinapis alba, although this assumption needs further study. Since the nectar of buckwheat and Sinapis alba is accessible for D. semiclausum, these plant species may also provide food for these parasitoids (Winkler in prep.). Further studies are required to explain similarities in the distribution pattern of Diadegma spp. to that of its host and to see how far field margins exert their effects in adjacent crop fields.

312 Fig. 2. Mean (± SE) number of diamondback moth caught in traps placed high (above) and low (below) in Brussels sprout fields, at different distances from the border. Grey bars are fields with flowering margin, white bars are fields without flowers in the second sampling period. Table 3. Statistics (General Linear Model) on the effects of type of field margin, trap position, distance from edge of field and trap line on numbers of Diadegma spp. in the first (above) and second (below) sampling periods. Non-significant interactions are omitted from the model. Source of variation Type III SS df MS F P Field edge 0.08 1 0.08 0.161 0.689 Position 20.32 1 20.32 42.59 <0.0001 Distance 9.41 3 3.14 6.57 0.0005 Trap Line 2.44 2 1.22 2.56 0.0833 Position x Distance 9.85 3 3.28 6.88 0.0003 Error 40.56 85 0.48 Source of variation Type III SS df MS F P Field edge 21.69 1 21.69 33.16 <0.0001 Position 63.65 1 63.65 97.31 <0.0001 Distance 17.14 3 5.71 8.73 <0.0001 Trap Line 0.47 2 0.23 0.36 0.7016 Field edge x 5.62 1 5.62 8.59 0.0044 Position Position x Distance 23.57 3 7.86 12.01 <0.0001 Error 54.94 84 0.65

313 Fig. 3. Mean (± SE) number of Diadegma spp. caught in traps placed high (above) and low (below) in Brussels sprout fields, at different distances from the border. Grey bars are fields with flowering margin, white bars are fields without flowers in the first sampling period. Inside the field, traps at a lower position (level of canopy) caught consistently more individuals (Table 3, Fig. 3). Within-field distribution of catches of wasps suggest that this species is indeed a specialist in cruciferous habitats and its flight activity within the crop is restricted to the plant canopy. These results show that flowering field margins may act as trap crop by attracting pest populations. However, trap crops may increase pest problems in adjacent fields when not accompanied by appropriate management practices (Hokkanen, 1991). Therefore the floral composition of field margins is an important factor to establish pest suppressive habitats, and management practices should be adjusted accordingly. Differences in the vertical position of traps have a great impact on efficiency of catches, and may influence reliability of detection and estimation of herbivore and parasitoid populations. Acknowledgements This project is financed by the Netherlands Organisation for Scientific Research (NWO- ALW, project number: 014-22.031). The help of Yde Jongema in the identification of insect material is acknowledged. The authors thank the experimental farm of Wageningen University and Research Centre (UNIFARM) for the maintenance of the experimental fields.

314 References Baggen, L.R., Gurr, G.M. and Meats, A. 1999. Flowers in tri-trophic systems: mechanisms allowing selective exploitation by insect natural enemies for conservation biological control. Entomol. Exp. Appl. 91: 155-161. Bowie, M.H., Gurr, G.M., Hossain, Z., Baggen, L.R. and Frampton, C.M. 1999. Effects of distance from field edge on aphidophagous insects in a wheat crop and observations on trap design and placement. Int. J. Pest Manage. 45: 69-73. Charleston, D.S. and Kfir, R. 2001. The possibility of using Indian mustard, Brassica juncea, as a trap crop for the diamondback moth, Plutella xylostella, in South Africa. Crop Prot. 19: 455-460. Fox L.R. and Eisenbach J. 1992. Contrary choices: possible exploitation of enemy-free space by herbivorous insects in cultivated vs. wild crucifers. Oecologia. 89: 574-579. Frei, G. and Manhart, C. 1992. Nützlinge und Schädlinge an künstlich angelegten Ackerkrautstreifen in Getreidefeldern. Verlag Paul Haupt, Bern: 140 pp. Hokkanen, H.M.T. 1991. Trap cropping in pest management. Annu. Rev. Entomol. 36: 119-38. Landis, D.A., Wratten, S.D. and Gurr, G.M. 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45: 175-201. Palaniswamy, P. and Gillot, C. 1986. Attraction of diamondback moths, Plutella xylostella (L.) (Lepidoptera: Plutellidae), by volatile compounds of canola, white mustard, and faba bean. Can. Entomol. 118: 1279-1285. Talekar, N.S. and Shelton, A.M. 1993. Biology, ecology, and management of the Diamondback moth. Annu. Rev. Entomol. 38: 275-301. Vet, L.E.M. and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37: 141-172. Waage, J. K. 1983. Aggregation in field parasitoid populations: foraging time allocation by a population of Diadegma (Hymenoptera: Ichneumonidae). Ecol. Entomol. 8: 447-453.