Mirid Bugs as Biological Control Agents in Protected Tomato Crops in the Oeste Region

Transcription

1 Mirid Bugs as Biological Control Agents in Protected Tomato Crops in the Oeste Region E. Figueiredo 1, R. Prieto 1, A. Mexia 1, S. Rodrigues 2, C.A. Costa 3 and M.C. Godinho 4 1 CEER, Instituto Superior Agronomia/UTL, Tapada da Ajuda, Lisboa, Portugal 2 Mariquita da Viola, Lda., Rua 8 Setembro, 11 Casalinhos de Alfaiata, Silveira, Portugal 3 ESAV/IPV, Quinta da Alagoa, Estrada de Nelas, Viseu, Portugal 4 ESAV/IPV and ESAS/IPS, Quinta do Galinheiro, Salvador Santarém, Portugal Keywords: conservation biological control, whiteflies, Trialeurodes vaporariorum Abstract The whitefly Trialeurodes vaporariorum is a key pest of greenhouse tomato crops in the Portuguese Oeste region. Mirids, tiger-fly and parasitoids are important biological control agents for this pest. Mirids are generalist predators and they control also the leafminers Liriomyza spp., and more recently the tomato leaf miner moth, Tuta absoluta. Preliminary studies to evaluate the impact of these predators were made on tomato crops in two commercial greenhouses during two years. Biological control had already been adopted for three years in one of these greenhouses (Greenhouse 1). In the other greenhouse (Greenhouse 2) biological control was initiated in the first year of this study. In both cases biological control consisted on augmentation of the autochthonous populations of natural enemies and improving them through augmentative releases whenever necessary. In the first year, differences among greenhouses regarding whitefly, sooty mould and mirids incidence were observed. For this pest, either chemical or biological treatments with mirids were not needed in Greenhouse 1. However, in Greenhouse 2 Macrolophus caliginosus was released for the control of whiteflies but it did not succeed due to the insecticides used for thrips control. Re-colonization by authoctonous Dicyphus cerastii was later observed in Greenhouse 2. In the second year, mirids population increased in Greenhouse 2 and at the end of the winter-spring crop mirid populations were already similar in size in both greenhouses. Whitefly and sooty mould incidences were also similar. In this crop M. caliginosus and D. cerastii were dominant in Greenhouse 1 and Greenhouse 2, respectively, but in the summer-autumn crop M. caliginosus and D. cerastii in the beginning and Nesidiocoris tenuis at the end were the dominant species in both greenhouses. INTRODUCTION Tomato is one of the main vegetable protected crops in Portugal. Whiteflies (Trialeurodes vaporariorum (West.) and Bemisia tabaci (Genn.)) are key-pests due to the direct and indirect (TYLCV transmission) damage on crops and to the frequent chemical treatments commonly applied with the consequent residues and pest resistance development. Biological control improvement allowed increasing food safety and protection of the environment. Some mirids are important predators. In the Mediterranean basin they colonize the crops spontaneously (Albajes and Alomar, 1999; Alomar et al., 2002; Castañé et al., 2004) when they are not often sprayed with pesticides. They are very efficient in whitefly control in tomato and other crops (Malausa et al., 1987; Gerling et al., 2001). Since they are polyphagous they can also feed on other pests as aphids, leafminers, thrips, mites and lepidopteran eggs and small larvae, contributing also to their control (Foglar et al., 1990; Izquierdo et al., 1994; Agustí et al., 1999; Albajes and Alomar, 1999; Ceglarska, 1999; Perdikis et al., 2002; Arnó et al., 2003; Blaeser et al., 2004). We found predation on larvae of South American tomato moth, Tuta absoluta (Meyrick), by mirids on protected tomatoes in the Oeste region (data not shown) and suitability of this prey to mirids was demonstrated by Urbaneja et al. (2009). The species found in tomato crops belong to the Proc. XXVIII th IHC IS on Greenhouse 2010 and Soilless Cultivation Ed.: N. Castilla Acta Hort. 927, ISHS

2 genus Macrolophus, Dicyphus and Nesidiocoris (Goula et al., 2002). These native predators play an important role on keeping the whitefly populations below the economical threshold level (Castañe and Gabarra, 2003). In Europe, Macrolophus caliginosus Wagner and Nesidiocoris tenuis (Reuter) are commercialized, mainly for whitefly control in protected crops. Dicyphinae species have been studied for their role as biological control agents on vegetable crops: M. caliginosus in France, Spain and Israel (Malausa et al., 1987; Albajes and Alomar, 1999; Gerling et al., 2001), Macrolophus pygmaeus (Rambur) in Greece (Perdikis and Lykouressis, 2000) and Spain (Urbaneja et al., 2009), Dicyphus hesperus Knigt in Canada (McGregor et al., 1999) and Northern Europe (Hatherly et al., 2008), Dicyphus hyalinipennis Burmeister in Hungary (Ceglarska, 1999), Dicyphus tamaninii Wagner in Spain (Lucas and Alomar, 2002), N. tenuis in the Canary Islands (Carnero et al., 2000) and Philippines (Torreno, 1994) and N. tenuis and Dicyphus errans Wolff in Italy (Tavella et al., 1997). In Portugal, N. tenuis and Macrolophus sp. in Madeira Island (Aguiar, 1999; Félix, 1999) and Dicyphus cerastii Wagner (Carvalho, 1999; Carvalho and Mexia, 2000) in the Portuguese mainland have been observed as important autochthonous predators in protected crops. D. cerastii, and/or eventually D. umbertae Sanchez & Cassis (Sanchez et al., 2006), is well adapted to the Oeste region. It is important to evaluate its predatory impact and to understand the interactions that are established with other generalist predators (e.g. the released M. caliginousus) and specific parasitoids (e.g.: Encarsia formosa Gahan) which are widely used as biological control agents on protected crops. MATERIALS AND METHODS The assays were performed in two nearby commercial greenhouses of the Hortipor company at Sobreiro Curvo (Torres Vedras) in the Oeste region, in 2005 and 2006: Greenhouse 1 (0.9 ha) under biological control for the last 3 years and Greenhouse 2 (0.7 ha) with biological control being implemented in the first year of this study. In both cases biological control consisted on augmentation of the autochthonous populations of natural enemies and improving them through mirid or parasitoid augmentative releases whenever necessary. Both greenhouses are composed by several metallic bodies, with 4m height and overhead (zenithal) opening in each body and lateral windows covered by a net for preventing bumblebees to go out. Roofs are made of polyethylene plastic film. Plants were soillessly grown, in rockwool plugs on slabs put on uncovered soil. Bumblebees, Bombus terrestris (L.), were used for pollination. Weekly, 4-5 leaves per plant on 30 plants on each greenhouse were sampled and inspected for whiteflies (nymphs and adults), mirids (nymphs and adults) and sooty mould. In the first year mirids were counted. In the second year only incidence (number of plants where they were present/total number observed plants) was registered. Incidence was also recorded for whiteflies and sooty mould. Other pests incidence was also recorded. The tiger-fly, Coenosia attenuata Stein, a whitefly and leafminer adult predator was also recorded. Winter-spring (Jan.-Jun.) and summer-autumn (Jul.-Dec.) crops were monitored. For the comparisons between pest and mirid incidences/numbers the paired samples t-test or the non-parametric Wilcoxon signed-rank test were performed using SPSS 17.0, after testing their assumptions. RESULTS AND DISCUSSION Whiteflies were the most important pest regarding incidence in all crops observed. Unlike Algarve and Alentejo where B. tabaci is important, in the Oeste region only T. vaporariorum is normally observed. Notice that the assays were performed before T. absoluta arrival (which occurred in July 2009). Thrips, leafminers, aphids and caterpillars were minor pests except in the first year and in the beginning of the winter-spring season in the Greenhouse 2 where the high thrips population imposed chemical applications. In the first year, differences between the greenhouses regarding whitefly, sooty mould and mirid incidence were detected although with no statistical significance for whitefly and sooty mould incidences (whitefly: t=-0.606, df=26, p=0.550; sooty mould: N=27, Z= 254

3 -1.576, p=0.115) but significant for total mirid number (N=27; Z=-4.036; p<0.001), number of mirid nymphs (N=27; Z=-3.285; p=0.001) and number of M. caliginosus adults (N=27; Z=-3.883; p<0.001) but not for the number of Dicyphus spp. adults (N=27; Z=-1.109; p=0.268). Incidence is an indirect way of measuring population density when whitefly population is not too high since whitefly rapidly colonizes all greenhouse area. However, for high whitefly populations incidence does not illustrate the population real size. High incidences can be reached with medium-high whitefly population levels; very high incidence can be reached with high population levels or very high population levels. Sooty mould can be a tool for distinguish between these situations. In the first year of this study, incidences of whitefly and sooty mould were not statistically different but population levels were quite different, being higher in Greenhouse 2. In Greenhouse 1 whitefly population was high since the beginning of the season; in Greenhouse 2 whitefly population was very low in the beginning but rapidly rose until 100% incidence (Fig. 1). Since sooty mould rose in Greenhouse2 and mirid incidence was low, M. caliginosus was released once in this greenhouse in the first year. Parasitoid releases (Encarsia formosa + Eretmocerus eremicus Rose & Zolnerowich) were done in both greenhouses to help mirids in the whitefly control. The insecticides used in Greenhouse 2 for thrips control (abamectine and acrinatrine) are very toxic to mirids. Therefore, M. caliginosus releases were not successful and mirids were present only on a few plants during all August (Fig. 1 and 2). Re-colonization by the authoctonous Dicyphus cerastii was later observed in Greenhouse 2 from outside crops and/or surrounding natural vegetation as seen by Alomar et al. (2002) and Castañé et al. (2004) for other mirid species. Mirid number was high all over the season in Greenhouse 2. In the second year, in winter-spring crop, whitefly incidence was high in both greenhouses. In Greenhouse 1 mirid incidence was about 40% in the beginning of the season and rose to 100% at the end of that season (Fig. 3). In Greenhouse 2, mirid population was very low in the beginning, being the incidence null until the end of April but at the end of the winter-spring crop the incidence was similar to that observed in Greenhouse 1 (Fig. 3) and mirids were well established in both greenhouses in the summer-autumn season (Fig. 4). In this season sooty mould was not seen on the observed leaves in both greenhouses (Fig. 3). In August, in Greenhouse 1 two abamectine applications for thrips control induced a high decrease in mirid incidence for 40%, recovering the mirid population in a week time to 70% and after two weeks to 90% (Fig. 3 and 4). In Greenhouse 2 only one application was made and so the decrease was not so severe. Significant differences between the two greenhouses were found in number of plants with mirids (N=33; Z=-2.256; p=0.024), especially in the winter-spring season (N=18; Z=-3.727; p<0.001), being the medians higher in Greenhouse 2. Fungicide applications were done through the two seasons in both years and greenhouses mainly to control grey mould Botrytis cinerea (Pers.), but apparently they were not so harmful to mirids. Significant differences regarding the whiteflies and sooty mold were not detected. In 2006, M. caliginosus and D. cerastii were dominant in Greenhouse 1 and Greenhouse2, respectively in the winter-spring season (data not shown), but in the summer-autumn crop M. caliginosus and D. cerastii, in the beginning, and Nesidiocoris tenuis, at the end, were the dominant species in both greenhouses (Fig. 4). Although, the mirids control well whitefly population they are zoophytophagous and they can damage tomato fruits (Albajes and Alomar, 1999; Lucas and Alomar, 2002; Arnó et al., 2010). However, phytophagous character varies among mirid species (Lucas and Alomar, 2002) and is a result of a balance between whitefly population and mirid population densities (Sanchez, 2009) and mirid intraguild predation (Lucas and Alomar, 2002). The typical punctures were rarely seen in the two greenhouses probably because the species present are more zoophagous and they had enough prey to feed on. Based on our observations it seems that N. tenuis is more easily phytophagous than D. cerastii or M. caliginosus in Oeste region conditions. 255

4 The tiger-fly was rarely seen since sampling was based on visual observation of tomato leaves and this predator is normally standing on the tutor in this crop (Prieto et al., 2005; Pinho et al., 2009). Even in preying they fly to catch the prey and then they return to the plant tutor, being rarely seen on the tomato leaves. From our experiments we realize that mirids need at least a season to become well established in a greenhouse structure and stabilized populations usually recover in a fortnight time after an intermediate toxic/ toxic chemical spraying. ACKNOWLEDGEMENTS We thank the Hortipor for allowing performing the assays in the company s greenhouses. This study was supported by the national research project AGRO 545. Literature Cited Agustí, N., Aramburu, J. and Gabarra, R Immunological detection of Helicoverpa armigera (Lepidoptera: Noctuidae) ingested by heteropteran predators: time-related decay and effect of meal size on detection period. Ann. Entomol. Soc. Am. 92: Albajes, R. and Alomar, O Current and potential use of polyphagous predators, p In: R. Albajes, M.L. Gullino, J.C. van Lenteren and Y. Elad (eds.), Integrated Pest and Disease Management in Greenhouse Crops, Kluwer, Dordrecht. Alomar, O., Goula, M. and Albajes R Colonisation of tomato fields by predatory mirid bugs (Hemiptera: Heteroptera) in northern Spain. Agric. Ecosyst. Environ. 89: Arnó, J., Alonso, E. and Gabarra, R Role of the parasitoid Diglyphus isaea (Walker) and the predator Macrolophus caliginosus Wagner in the control of leafminers. IOBC/wprs Bull. 26: Arnó, J., Castañé, C., Riudavets, J. and Gabarra, R Risk of damage to tomato crops by the generalist zoophytophagous predator Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae). Bull. Entomol. Res. 100: Blaeser, P., Sengonca, C. and Zegula, T The potential use of different predatory bug species in the biological control of Frankliniella occidentalis (Pergande) (Thysanoptera:Thripsidae). J. Pest. Sci. 77: Carnero, A., Diaz, S., Amador, S. Hernández, M. and Hernández. E Impact of Nesidiocoris tenuis Reuter (Hemiptera: Miridae) on whitefly populations in protected tomato crops. IOBC/wprs Bull. 23(1):259. Carvalho, P Os mirídeos e a limitação natural na cultura protegida do tomateiro. MSc Thesis, ISA/UTL, Lisboa. Carvalho, P. and Mexia, A First approach on the potential role of Dicyphus cerastii Wagner (Hemiptera: Miridae), as natural control agent in Portuguese greenhouses. IOBC/wprs Bull. 23(1): Castañé, C., Alomar, O., Goula, M. and Gabarra, R Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii. Biol. Control 30: Ceglarska, E.B Dicyphus hyalinipennis Burm. (Heteroptera: Miridae) a potential biological control agent for glasshouse pests in Hungary. IOBC/wprs Bull. 22(1): Foglar, H., Malausa, J.C. and Wajnberg, E The functional response and preference of Macrolophus caliginosus (Heteroptera: Miridae) for two of its prey: Myzus persicae and Tetranychus urticae. Entomophaga, 35: Gerling, D., Alomar, O. and Arnó, J Biological control of Bemisia tabaci using predators and parasitoids. Crop Prot. 20: Goula, M., Alomar, O.C. and Castañe, C.C Predatory mirids in tomato crops. PartB. European Whitefly Studies Network, John Innes Centre, Norwich. ( Hatherly, I.S., Pedersen, B.P. and Bale, J.S Establishment potential of the predatory mirid Dicyphus hesperus in northern Europe. BioControl 53: Izquierdo, J.I., Solans, P. and Vitalle, J Parasitoids and predators of Helicoverpa 256

5 armigera (Hübner) on table tomato crops. Bol. Sanid. Veg. Plagas 20: Lucas, E. and Alomar, O Impact of Macrolophus caliginosus presence on damage production by Dicyphus tamaninii (Heteroptera: Miridae) on tomato fruits. J. Econ. Entomol. 95: Malausa, J.C., Drescher, J. and Franco, E Perspectives for the use of a predaceous bug Macrolophus caliginosus Wagner (Heteroptera: Miridae) on glasshouse crops. IOBC/wprs Bull. 10(2): McGregor, R.R., Gillespie, D.R., Park, C.G., Quiring, D.M.J. and Foisy, M.R.J Potential use of Dicyphus hesperus Knight (Heteroptera: Miridae) for biological control of pests of greenhouse tomatoes. Biol. Control 16: Perdikis, D.C. and Lykouressis, D.P Life table and biological characteristics of Macrolophus pygmaeus when feeding on Myzus persicae and Trialeurodes vaporariorum. Entomol. Exp. Appl. 102: Pinho, V., Mateus, C., Rebelo, M.T. and Kühne, S Distribuição espacial de Coenosia attenuata Stein (Diptera: Muscidae) e das suas presas em estufas de hortícolas na região Oeste, Portugal. Bol. San. Veg. Plagas 35: Prieto, R., Figueiredo, E., Miranda, C. and Mexia, A Coenosia attenuata Stein (Diptera: Muscidae): prospecção e actividade em culturas protegidas em Portugal. Bol. San. Veg. Plagas 31: Sanchez, J.A Density thresholds for Nesidiocoris tenuis (Heteroptera: Miridae) in tomato crops. Biol. Control 51: Sanchez, J.A., Martinez-Cascales, J.I. and Casssis, G Description of a new species of Dicyphus Fieber (Insecta: Heteroptera: Miridae) from Portugal based on molecular data. Insect Syst. Evol. 37: Tavella, L., Alma, A. and Sargiotto, C Samplings of Miridae Dicyphinae in tomato crops of Northwestern Italy. IOBC/wprs Bull. 20(4): Torreno, H Predation behaviour and efficiency of the bug Cyrtopeltis tenuis (Hemiptera: Miridae), against the cutworm, Spodoptera litura (F). Philipp. Entomol. 9: Urbaneja, A., Montón, H. and Molla, O Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J. Appl. Entomol. 133:

6 Figurese Fig. 1. Incidence of whiteflies, mirids and sooty mould in Greenhouse 1 and Greenhouse 2, in 2005 (winter-spring and summer-autumn crops). The arrows indicate the treatments for thrips control. Fig. 2. Mirids in Greenhouse 1 and Greenhouse 2, in 2005 number/30 plants (winter-spring and summer-autumn crops) (note the different scale of y-axis). 258

7 Fig. 3. Incidence of whiteflies, mirids and sooty mould in Greenhouse 1 and Greenhouse 2, in 2006 (winter-spring and summer-autumn crops). Fig. 4. Mirid incidence on tomato in Greenhouse 1 and Greenhouse 2, in 2006 (summer-autumn crop). 259

8 260