Biological Control of Aphids by the Predatory Midge Aphidoletes aphidimyza in the Presence of Intraguild Predatory Bugs and Thrips

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1 Biologial Control of Aphids by the Predatory Midge Aphidoletes aphidimyza in the Presene of Intraguild Predatory Bugs and Thrips G.J. Messelink a, C.M.J. Bloemhard and R. Vellekoop Wageningen UR Greenhouse Hortiulture P.O. Box 20, 2265 ZG Bleiswijk The Netherlands Keywords: Myzus persiae, Orius laevigatus, Orius majusulus, sweet pepper, intraguild predation, hyperpredation, apparent ompetition, mixed diets Abstrat In organially grown sweet peppers, aphids are the most important pest. The wide range of natural enemies of aphids, that are ommerially availle, is not a guarantee for suessful ontrol but rather an indiation that this problem is diffiult to takle. Strategies for ontrol vary among organi growers and it is still not known whih natural enemy omplexes give the best results. When releasing natural enemies for aphid ontrol, it is important to onsider the possible interations with other pest speies and natural enemies present. Within man-made natural enemy ommunities for multiple pest ontrol, diret and indiret interations our whih an enhane or disrupt biologial ontrol, suh as predators eating other predators, behavioural hanges, plant responses or apparent ompetition. Here we investigated the effets of the generalist predatory bugs Orius laevigatus and Orius majusulus on biologial ontrol of green peah aphids, Myzus persiae, by the predatory midge Aphidoletes aphidimyza in the sene or presene of thrips. Our results showed that intraguild predation of aphidophageous midges by generalist predatory bugs is a realisti phenomenon, but the risk of disruption of aphid ontrol seems to be limited. The addition of thrips and O. majusulus to predatory midges even enhaned the suppression of aphids. We onlude that a broad system view with predator-prey omplexes is required for identifying suessful natural enemy omplexes for aphid ontrol. INTRODUCTION Aphids are the most destrutive pest speies in organially grown sweet peppers. The green peah aphid, Myzus persiae (Sulzer), espeially the red phenotype, is notorious for its fast reprodution and tendeny to olonize flowers and young leaves. This behaviour diretly results in redution in growth of the plant and fruit prodution. Moreover, the honeydew sereted by these aphids pollutes leaves and fruit, whih onsequently failitates growth of sooty mould. Another damaging aphid speies in sweet pepper is the foxglove aphid, Aulaorthum solani (Kaltenbah). This speies typially indues strong plant responses suh as yellow neroti spots and leaf deformation, whih an our at low aphid densities. At higher densities, aphid-indued damage an result in leaf drop. Biologial ontrol of these aphids is mainly based on weekly releases of the parasitoids, Aphidius olemani Vierek and Aphidius ervi Haliday, and the predatory midge, Aphidoletes aphidimyza (Rondani). Additionally, growers release the slower reproduing wasps Aphelinus dominalis (Dalman) and hrysopid, syrphid or oinellid predators. Despite releases of mulitple natural enemies, bioontrol programs often do not sueed. One reason ould be that these natural enemies interat with bioontrol agents that are released to ontrol other pest speies, suh as generalist predatory mites and predatory bugs for the ontrol of thrips. We reently showed that predatory mites strongly disrupt the biologial ontrol of aphids using the predatory midge, A. aphidimyza, beause of hyperpredation of the midge eggs (Messelink et al., a Gerben.messelink@wur.nl Pro. First IC on Organi Greenhouse Hort. Eds.: M. Dorais and S.D. Bishop Ata Hort. 915, ISHS

2 2011). Another threat for predatory midges ould be the predation by generalist Orius bugs, whih are mainly used for ontrolling thrips. These predators are known to feed not only on thrips, but also on aphids and the aphidophagous predator A. aphidimyza (Christensen et al., 2002). Suh interations have been referred to as intraguild predation (Fig. 1), whih ours when one predator speies (the intraguild predator) kills and eats another predator speies (the intraguild prey) with whom it also ompetes for shared prey (Polis et al., 1989; Holt and Polis, 1997). In theory, intraguild predation an disrupt biologial ontrol (Rosenheim et al., 1995), but in pratie, results are mixed (Janssen et al., 2006, 2007; Vane-Chalraft et al., 2007). Here we examine the effets of Orius laevigatus (Fieber) and Orius majusulus (Reuter) on the biologial ontrol of aphids with predatory midges in the presene of thrips as an alternative prey for Orius. Furthermore, we disuss the role of speies interations in developing management strategies for aphid ontrol in sweet pepper. MATERIALS AND METHODS Rearing Sweet pepper plants, Capsium annuum L. Ferrari (Enza Zaden), were grown in rokwool bloks in a greenhouse ompartment. We used the red phenotype of the green peah aphid, M. persiae, whih was ultured on sweet pepper plants. Western flower thrips, Frankliniella oidentalis (Pergande), were ultured on flowering hrysanthemum plants, Mirimar. The predatory midge, A. aphidimyza, and predatory bug, O. laevigatus (Fieber), were obtained from Koppert Biologial Systems (Berkel en Rodenrijs, The Netherlands), whereas the predatory bug, O. majusulus, was obtained from Biobest NV (Westerlo, Belgium). Greenhouse Experiment A age experiment was arried out to assess the effets of predatory bugs on the suppression of aphids, in the presene of the predatory midge A. aphidimyza. Thrips were introdued to a subset of ages to provide an alternative prey for the predatory bugs. Individual flowering sweet pepper plants, a. height 30 m with leaves, were put into a single age (diameter 30 m, height 40 m, top with side-openings overed with inset gauze). Cages were plaed on tles and maintained, at an average of 21 C, in one greenhouse ompartment. The lower plant stem and roots in rokwool extended through a sealed hole at the bottom of the ages in order to allow automati supply of a standard nutrient solution with an ebb-and-flow system. There were 8 treatments, with 4 repliates per treatment: (1) aphids only, (2) aphids + O. laevigatus + thrips, (3) aphids + O. majusulus + thrips, (4) aphids + A. aphidimyza, (5) aphids + A. aphidimyza + O. laevigatus, (6) aphids + A. aphidimyza + O. majusulus, (7) aphids + A. aphidimyza + O. laevigatus + thrips and (8) aphids + A. aphidimyza + O. majusulus + thrips. Eah plant was infeted with 20 aphids of mixed age, whih were olleted with a fine brush from the ulture on sweet pepper. Adult thrips were introdued three times in the destined treatments in densities of 20, 20 and 40 females per plant after 1, 11 and 23 days post aphid release, respetively. Repeated releases of thrips were neessary beause thrips proved to be ontrolled effetively. The predatory midge A. aphidimyza was introdued 10 days after aphid release by adding 10 pupae per age in humid vermiulite. The adult midges emerged within 4 to 7 days, and no mortality of pupae was observed. Ten adult female predatory bugs were introdued 17 days after aphid release in eah age. The densities of all insets were assessed one, 28 days after aphid release, by heking all parts of eah plant under a stereomirosope (40x). For statistial analyses, we performed a standard ANOVA on the log transformed densities of insets. Differenes among treatments were tested at the 5% level using Fisher s Least Signifiant Differene (LSD) method. 172

3 RESULTS AND DISCUSSION Densities of the predatory midge were signifiantly redued (F 4,19 = 4.14, p = 0.019) in the presene of predatory bugs, suggesting intraguild predation. For O. majusulus, this effet was only signifiant when thrips were also present (Fig. 2). We also observed dead and empty suked midge larvae in the treatments with predatory bugs. The presene of thrips did not signifiantly affet the extent of intraguild predation by either Orius speies (Fig. 2). Aphid densities were also signifiantly affeted by the treatments (F 7,31 = , p<0.001). The addition of predatory bugs and thrips redued aphid densities slightly, but the trend was not found to be signifiant. The predatory midge alone or when present with either Orius sp. showed a lear ontrol of aphids (Fig. 3). The addition of Orius bugs to ages ontaining predatory midges did not result in signifiant inreases of aphid densities (Fig. 3). The presene of thrips did not affet the ombined effet of O. laevigatus and predatory midges on aphids. However, the presene of thrips signifiantly inreased the ontrol of aphids by O. majusulus and predatory midges ompared with the ombined treatment of these predators without thrips (Fig. 3). The omposition of prey (aphids, thrips, midges) signifiantly affeted the final densities of O. majusulus and O. laevigatus (F 5,23 = 3.97, p=0.013) (Fig. 4). DISCUSSION In this study, we learly demonstrate that both O. majusulus and O. laevigatus an signifiantly redue densities of the aphid predator A. aphidimyza. The results with O. majusulus onfirm earlier observations (Christensen et al., 2002). However, the observed intraguild predation in our study did not signifiantly disrupt the ontrol of aphids by the predatory midge. It ould be that redued densities of midge larvae were not only ounterbalaned by aphid predation by the predatory bugs, but also by inreased predation rates of the remaining midge larvae beause it has been observed that larvae of A. aphidimyza inrease predation ativity at higher prey-predator ratios (Markkula et al., 1979). Although to date most studies on intraguild predation have not aounted for the effets of alternative prey, reent theoretial models have shown that the presene of alternative prey influene the effets of intraguild predation in various ways (Holt and Huxel, 2007). Thrips are a suitle prey for Orius bugs, but in the ase of O. laevigatus, we ould not detet any influene of thrips on intraguild predation. Surprisingly, we found improved ontrol of aphids when thrips were added to the ombined treatment of O. majusulus and predatory midges. Several underlying interations might explain the results. One explanation for a better ontrol of aphids with predatory midges and O. majusulus in the presene of thrips ould be that thrips inrease Orius densities, whih onsequently an inrease the predator s effets on aphids. Suh a predator-mediated pest interation has been referred to as apparent ompetition (Holt, 1977) and was shown to enhane pest ontrol (Messelink et al., 2008). We did not find evidene for this effet in our study beause we did not inlude ontrol treatments with only predatory bugs and aphids. However, we observed inreased densities of O. laevigatus with inreased prey diversity, suggesting a positive effet of inreased prey numbers on the reprodution of Orius bugs (a. 90% of the final populations were juveniles). However, in the ase of O. laevigatus, aphids were present in suffiient numbers (at least >50 aphids/predator) in all treatments. This suggests that inreased reprodution might not only be aused by the presene of more food, but also by a better performane of the predators on a mixed diet. The lower final densities of O. majusulus in the treatment with predatory midges + aphids + thrips might be explained by food depletion beause in this treatment aphids were suppressed to low numbers (Fig. 4). In the treatments with thrips, another possible mehanism may have involved behavioural hanges of the predatory bugs in presene of multiple prey; so-alled traitmediated effets (Prasad and Snyder, 2006). For example, it ould be that the presene of 173

4 A. aphidimyza larvae inreased the predation of predatory bugs on aphids by hanging foraging ativity. Other studies showed that the aphid predators Harmonia axyridis Pallas and Coinella septempuntata L. ate more apple aphids when leafroller larvae were present (Luas et al., 2004). Likewise, when provided with fruit flies, the arid, Bembidion lampros (Herbst), ate more ereal aphids (Madsen et al., 2004). The generalist predators Nis spp. ate signifiantly more aphids when eggs of the Colorado potato beetle were availle, ompared with an environment where there were no alternative prey present (Koss et al., 2004). We suggest that suh mixed prey effets on predator behaviour and predator development deserve more attention in future researh with generalist predators in greenhouses. CONCLUSIONS Intraguild predation of aphidophageous midges by generalist predatory bugs is a realisti phenomenon, but the risk of disruption of aphid ontrol seems to be limited. The addition of thrips and O. majusulus to predatory midges even enhaned the suppression of aphids. Thus, this predator seems to be a promising natural enemy for multiple pest ontrol. For further development of bioontrol programs, we suggest the importane of evaluating natural enemies within a ontext of realisti ommunities of pests and predators. This broader view of a system will ontribute in identifying natural enemy omplexes that will ontrol both aphids and thrips in rops. ACKNOWLEDGEMENTS This study was funded by the Duth Ministry of Agriulture, Nature and Food Quality. Koppert Biologial Systems and Biobest are thanked for supplying the natural enemies. Literature Cited Christensen, R.K., Enkegaard, A. and Brødsgaard, H.F Intraspeifi interations among the predators Orius majusulus and Aphidoletes aphidimyza. IOBC/wprs Bulletin 25: Holt, R.D Predation, apparent ompetion and the struture of prey ommunities. Theoretial Population Biology 12: Holt, R.D. and Polis, G.A A theoretial framework for intraguild predation. Amerian Naturalist 149: Holt, R.D. and Huxel, G.R Alternative prey and the dynamis of intraguild predation: Theoretial perspetives. Eology 88: Janssen, A., Montserrat, M., HilleRisLambers, R., de Roos, A.M., Pallini, A. and Selis, M.W Intraguild predation usually does not disrupt biologial ontrol. p In: J. Brodeur and G. Boivin (eds.), Trophi and Guild in Biologial Interations Control, Vol. 3. Springer SBS, Dordreht, Netherlands. Janssen, A., Selis, M.W., Magalhães, S., Montserrat, M. and van der Hammen, T Hitat struture affets intraguild predation. Eology 88: Koss, A.M., Chang, G.C. and Snyder, W.E Predation of green peah aphids by generalist predators in the presene of alternative, Colorado potato beetle egg prey. Biologial Control 31: Luas, E., Demougeot, S., Vinent, C. and Coderre, D Predation upon the obliquebanded leafroller, Choristoneura rosaeana (Lepidoptera: Tortriidae), by two aphidophagous oinellids (Coleoptera: Coinellidae) in the presene and sene of aphids. European J. of Entomology 101: Madsen, M., Terkildsen, S. and Toft, S Miroosm studies on ontrol of aphids by generalist arthropod predators: Effets of alternative prey. Bioontrol 49: Markkula, M., Tiitanen, K., Hamalainen, M. and Forsberg, A The aphid midge Aphidoletes aphidimyza (Diptera, Ceidomyiidae) and its use in biologial ontrol of aphids. Annales Entomologii Fennii 45: Messelink, G.J., Bloemhard, C.M.J., Cortes, J.A., Selis, M.W. and Janssen, A

5 Hyperpredation by generalist predatory mites disrupts biologial ontrol of aphids by the aphidophagous gall midge Aphidoletes aphidimyza. Biologial Control 57: doi /j.bioontrol Messelink, G.J., van Maanen, R., van Steenpaal, S.E.F. and Janssen, A Biologial ontrol of thrips and whiteflies by a shared predator: Two pests are better than one. Biologial Control 44: Polis, G.A., Myers, C.A. and Holt, R.D The eology and evolution of intraguild predation: Potential ompetitors that eat eah other. Annual Review of Eology and Systematis 20: Prasad, R.P. and Snyder, W.E Diverse trait-mediated interations in a multipredator, multi-prey ommunity. Eology 87: Rosenheim, J.A., Kaya, H.K., Ehler, L.E., Marois, J.J. and Jaffee, B.A Intraguild predation among biologial ontrol agents: Theory and evidene. Biologial Control 5: Vane-Chalraft, H.D., Rosenheim, J.A., Vonesh, J.R., Osenberg, C.W. and Sih, A The influene of intraguild predation on prey suppression and prey release: A metaanalysis. Eology 88: Figures A generalist predatory mites B generalist predatory bugs predatory midge Aphidoletes aphidimyza predatory midge Aphidoletes aphidimyza thrips aphids thrips aphids plant plant Fig. 1. Food webs showing the differene between hyperpredation (A) and intraguild predation (B). 175

6 Midge + O. laevigatus + thrips b Midge + O. majusulus + thrips b Midge + O. laevigatus Midge + O. majusulus Midge a Predatory midge density Fig. 2. Effets of predatory bugs on densities of the predatory midge A. aphidimyza in the presene or sene of thrips. Shown are average (±SE) densities of larvae per plant. Different letters indiate signifiant differenes among treatments (Fisher s LSD test, p<0.05). Midge + O. laevigatus + thrips Midge + O. majusulus + thrips d Midge + O. laevigatus b Midge + O. majusulus Midge O. laevigatus + thrips O. majusulus + thrips Control a Aphid density Fig. 3. Effets of predatory bugs on the suppression of aphids by the predatory midge A. aphidimyza in the presene or sene of thrips. Shown are average (±SE) densities of the aphid M. persiae per plant. Different letters indiate signifiant differenes among treatments (Fisher s LSD test, p<0.05). 176

7 Predator density aphids + thrips aphids + midges aphids + midges + thrips b b a O. majusulus O. laevigatus Fig. 4. Performane of predatory bugs on sweet pepper plants with different mixtures of the prey speies. Shown are the average densities (±SE) of adults + nymphs per plant. Different letters indiate signifiant differenes among treatments (Fisher s LSD test, p<0.05). 177

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