Abstract
Frankliniella occidentalis is a major pest in agriculture. Problems with its control are mainly due to pupation in the soil and resistance to insecticides. Biological control agents (BCA) can be used against thrips pests as an alternative to conventional insecticides. We evaluated the effectiveness of a number of BCA for control of F. occidentalis in cyclamen under greenhouse conditions. Three BCA (Amblyseius swirskii, Neoseiulus californicus and Orius laevigatus) were applied to the canopy and two (Macrocheles robustulus and Steinernema feltiae) to the soil in single and combined releases. Results showed that applications of predatory mites and nematodes achieved good control of F. occidentalis. Unsatisfactory control was obtained using O. laevigatus. The use of nematodes determined the extinction of thrips, but with a delay. The combination of nematodes in the soil and predatory mites in the canopy caused a more prompt reduction of thrips in flowers.
Similar content being viewed by others
References
Allen WR, Matteoni JA (1988) Cyclamen ringspot: epidemics in Ontario greenhouses caused by the tomato spotted wilt virus. Can J Plant Pathol 10:41–46
Ansari MA, Brownbridge M, Shah FA, Butt TM (2008) Efficacy of entomopathogenic fungi against soil-dwelling life stages of western flower thrips, Frankliniella occidentalis, in plant-growing media. Entomol Exp Appl 127:80–87
Arthurs S, Heinz KM (2006) Evaluation of nematodes Steinernema feltiae and Thripinema nicklewoodi as biological control agents of western flower thrips Frankliniella occidentalis infesting Chrysanthemum. Biocontrol Sci Technol 16:141–155
Arthurs S, McKenzie CL, Chen J, Dogramaci M, Brennan M, Houben K, Osborne L (2009) Evaluation of Neoseiulus cucumeris and Amblyseius swirskii (Acari: Phytoseiidae) as biological control agents of chilli thrips, Scirtothrips dorsalis (Thysanoptera: Thripidae) on pepper. Biol Control 49:91–96
Bakker FM, Sabelis MW (1989) How larvae of Thrips tabaci reduce the attack success of phytoseiid predators. Entomol Exp Appl 50:47–51
Beerling E (2008) The switch to IPM in cut-chrysanthemum in the Netherlands. IOBC/WPRS Bull 32:17–20
Berndt O, Meyhöfer R, Poehling HM (2004) The edaphic phase in the ontogenesis of Frankliniella occidentalis and comparison of Hypoaspis miles and Hypoaspis aculeifer as predators of soil-dwelling thrips stages. Biol Control 30:17–24
Broadbent AB, Rhainds M, Shipp L, Murphy G, Wainman L (2003) Pupation behaviour of western flower thrips (Thysanoptera: Thripidae) on potted chrysanthemum. Can Entomol 135:741–744
Brødsgaard HF (1994) Insecticide resistance in European and African strains of western flower thrips (Thysanoptera: Thripidae) tested in a new residue-on-glass test. J Econ Entomol 87:1141–1146
Brødsgaard F, Enkegaard A (2005) Intraguild predation between Orius majusculus (Reuter) (Hemiptera: Anthocoridae) and Iphiseius degenerans Berlese (Acarina: Phytoseiidae). IOBC/WPRS Bull 28:19–22
Brownbridge M, Saito T, Buitenhuis R, Brommit A, Murphy G (2011) Developing a biologically-based IPM program for western flower thrips, Frankliniella occidentalis, in greenhouse floriculture. IOBC/WPRS Bull 68:21–24
Brownbridge M, Saito T, Côté P (2014) Considerations and combinations to improve control of pupating western flower thrips in chrysanthemums. IOBC/WPRS Bull 102:29–35
Buitenhuis R, Shipp JL (2005) Efficacy of entomopathogenic nematode Steinernema feltiae (Rhabditida: Steinernematidae) as influenced by Frankliniella occidentalis (Thysanoptera: Thripidae) developmental stage and host plant stage. J Econ Entomol 98:1480–1485
Buitenhuis R, Shipp JL (2008) Influence of plant species and plant growth stage on Frankliniella occidentalis pupation behavior in greenhouse ornamentals. J Appl Entomol 132:86–88
Buitenhuis R, Shipp L, Scott-Dupree C (2010) Intra-guild vs extra-guild prey: effect on predator fitness and preference of Amblyseius swirskii (Athias-Henriot) and Neoseiulus cucumeris (Oudemans) (Acari: Phytoseiidae). Bull Entomol Res 100:167–173
Buitenhuis R, Shipp L, Scott-Dupree C, Brommit A, Lee W (2014) Host plant effects on the behaviour and performance of Amblyseius swirskii (Acari: Phytoseiidae). Exp Appl Acarol 62:171–180
Chow A, Chau A, Heinz KM (2008) Compatibility of Orius insidiosus (Hemiptera: Anthocoridae) with Amblyseius (Iphiseius) degenerans (Acari: Phytoseiidae) for control of Frankliniella occidentalis (Thysanoptera: Thripidae) on greenhouse roses. Biol Control 44:259–270
Chow A, Chau A, Heinz KM (2010) Compatibility of Amblyseius (Typhlodromips) swirskii (Athias-Henriot) (Acari: Phytoseiidae) and Orius insidiosus (Hemiptera: Anthocoridae) for biological control of Frankliniella occidentalis (Thysanoptera: Thripidae) on roses. Biol Control 53:188–196
Cloyd RA (2009) Western flower thrips (Frankliniella occidentalis) management on ornamental crops grown in greenhouses: have we reached an impasse. Pest Technol 3:1–9
Cocuzza GE, De Clercq P, Veire M, Cock A, Degheele D, Vacante V (1997) Reproduction of Orius laevigatus and Orius albidipennis on pollen and Ephestia kuehniella eggs. Entomol Exp Appl 82:101–104
Coll M, Ridgway RL (1995) Functional and numerical responses of Orius insidiosus (Heteroptera: Anthocoridae) to its prey in different vegetable crops. Ann Entomol Soc Am 88:732–738
Cuthbertson AG, Mathers JJ, Croft P, Nattriss N, Blackburn LF, Luo W, Walters KF (2012) Prey consumption rates and compatibility with pesticides of four predatory mites from the family Phytoseiidae attacking Thrips palmi Karny (Thysanoptera: Thripidae). Pest Manag Sci 68:1289–1295
de Courcy Williams M (2001) Biological control of thrips on ornamental crops: interactions between the predatory mite Neoseiulus cucumeris (Acari: Phytoseiidae) and western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), on cyclamen. Biocontrol Sci Technol 11:41–55
Ebssa L, Borgemeister C, Berndt O, Poehling H (2001) Efficacy of entomopathogenic nematodes against soil-dwelling life stages of western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae). J Invertebr Pathol 78:119–127
Goleva I, Zebitz CP (2013) Suitability of different pollen as alternative food for the predatory mite Amblyseius swirskii (Acari, Phytoseiidae). Exp Appl Acarol 61:259–283
Holmes ND, Bennison JA, Maulden KA, Kirk WD (2012) The pupation behaviour of the western flower thrips, Frankliniella occidentalis (Pergande). Acta Phytopathol Entomol Hung 47:87–96
Jacobson RJ (1997) Integrated pest management (IPM) in glasshouses. In: Lewis T (ed) Thrips as crop pests. CAB International Wallingford, UK, pp 639–666
Jacobson RJ, Croft P, Fenlon J (2001) Suppressing establishment of Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) in cucumber crops by prophylactic release of Amblyseius cucumeris Oudemans (Acarina: Phytoseiidae). Biocontrol Sci Technol 11:27–34
Karg W (1993) Raubmilben: Acari (Acarina), Milben, Parasitiformes (Anactinochaeta), Cohors Gamasina Leach. Die Tierwelt Deutschlands, Gustav Fischer, Stuttgart, Germany
Linnamäki M, Hulshof J, Vänninen I (1998) Biology and prospects for enhancing biocontrol of the western flower thrips Frankliniella occidentalis in cut roses. In: Proceedings 1998 Brighton crop protection conference—pests and diseases 2, British Crop Protection Council, Farnham, UK, pp 187–192
Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute Inc, Cary, USA
Lundgren JG (2011) Reproductive ecology of predaceous Heteroptera. Biol Control 59:37–52
Lundgren JG, Fergen JK, Riedell WE (2008) The influence of plant anatomy on oviposition and reproductive success of the omnivorous bug Orius insidiosus. Anim Behav 75:1495–1502
Manners AG, Dembowski BR, Healey MA (2013) Biological control of western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), in gerberas, chrysanthemums and roses. Aust J Entomol 52:246–258
McMurtry JA, De Moraes GJ, Sourassou UF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320
Messelink G, van Holstein-Saj R (2008) Improving thrips control by the soil-dwelling predatory mite Macrocheles robustulus (Berlese). IOBC/WPRS Bull 32:135–138
Messelink GJ, van Steenpaal SEF, Ramakers PMJ (2006) Evaluation of phytoseiid predators for control of western flower thrips on greenhouse cucumber. BioControl 51:753–768
Messelink GJ, Maanen RV, van Steenpaal SE, Janssen A (2008) Biological control of thrips and whiteflies by a shared predator: two pests are better than one. Biol Control 44:372–379
Norton AP, Belden E, English-Loeb G (2001) Host plant manipulation of natural enemies: leaf domatia protect beneficial mites from insect predators. Oecologia 126:535–542
Parrella MP, Jones VP (1987) Development of integrated pest management strategies in floricultural crops. Bull Entomol Soc Am 33:28–34
Premachandra WTSD, Borgemeister C, Berndt O, Ehlers RU, Poehling HM (2003) Combined releases of entomopathogenic nematodes and the predatory mite Hypoaspis aculeifer to control soil-dwelling stages of western flower thrips Frankliniella occidentalis. BioControl 48:529–541
Ranabhat NB, Goleva I, Zebitz CP (2014) Life tables of Neoseiulus cucumeris exclusively fed with seven different pollens. BioControl 59:195–203
Riley DG, Joseph SV, Srinivasan R, Diffie S (2011) Thrips vectors of tospoviruses. J Int Pest Manag 2:I1–I10
Riudavets J (1995) Predators of Frankliniella occidentalis (Perg.) and Thrips tabaci Lind.: a review, vol 95. Wageningen Agricultural University Papers, Wageningen, The Netherlands, pp 43–87
Skirvin D, Kravar-Garde L, Reynolds K, Jones J, De Courcy WM (2006) The influence of pollen on combining predators to control Frankliniella occidentalis in ornamental chrysanthemum crops. BioControl Sci Technol 16:99–105
Steiner MY, Spohr LJ, Goodwin S (2011) Relative humidity controls pupation success and dropping behaviour of western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Aust J Entomol 50:179–186
Tavella L, Arzone A, Alma A (1991) Researches on Orius laevigatus (Fieb.), a predator of Frankliniella occidentalis (Perg.) in greenhouses. A preliminary note. IOBC/WPRS Bull 14:65–72
Tixier MS, Baldassar A, Duso C, Kreiter S (2013) Phytoseiidae in European grape (Vitis vinifera L.): bioecological aspects and keys to species (Acari: Mesostigmata). Zootaxa 3721:101–142
Tommasini MG, Maini S (1995) Frankliniella occidentalis and thrips harmful to vegetable and ornamental crops in Europe. In: Loomans AJM, van Lenteren JC, Tommasini MG, Maini S, Riudavets J (eds) Biological control of thrips pests, Wageningen Agricultural University Papers, Wageningen, The Netherlands, pp 1–35
van de Veire M, Degheele D (1992) Biological control of the western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera, Thripidae), in greenhouse sweet peppers with Orius spp. (Hemiptera, Anthocoridae). A comparative study between O. niger (Wolff) O. insidiosus (Say). Biocontrol Sci Technol 2:281–283
van Driesche RG, Lyon S, Stanek EJ III, Xu B, Nunn C (2006) Evaluation of efficacy of Neoseiulus cucumeris for control of western flower thrips in spring bedding crops. Biol Control 36:203–215
van Houten YM, Ostlie ML, Hoogerbrugge H, Bolckmans K (2005) Biological control of western flower thrips on sweet pepper using the predatory mites Amblyseius cucumeris, Iphiseius degenerans, A. andersoni and A. swirskii. IOBC/WPRS Bull 28:283–286
van Lenteren JC (2000) A greenhouse without pesticides: fact or fantasy? Crop Prot 19:375–384
Weintraub PG, Pivonia S, Steinberg S (2011) How many Orius laevigatus are needed for effective western flower thrips, Frankliniella occidentalis, management in sweet pepper? Crop Prot 30:1443–1448
Whitfield AE, Ullman DE, German TL (2005) Tospovirus-thrips interactions. Annu Rev Phytopathol 43:459–489
Wiethoff J, Poehling HM, Meyhöfer R (2004) Combining plant-and soil-dwelling predatory mites to optimise biological control of thrips. Exp Appl Acarol 34:239–261
Wimmer D, Hoffmann D, Schausberger P (2008) Prey suitability of western flower thrips, Frankliniella occidentalis, and onion thrips, Thrips tabaci, for the predatory mite Amblyseius swirskii. Biocontrol Sci Technol 18:533–542
Zimmermann G (1986) The “Galleria bait method” for detection of entomopathogenic fungi in soil. J Appl Entomol 102:213–215
Acknowledgments
The authors thank “Gruppo Padana Ortofloricoltura dei F.lli Gazzola” for providing technical support to this study. The authors are grateful to Evangelia Chatzidimitriou, Anna Nicole Skourti and Andrea Raffagnato for the assistance during the experiment. The authors thank the editor and three anonymous reviewers for helpful comments on previous versions of the manuscript. This study has been partially funded by REG. (CE) N. 1698/05—Programma di sviluppo rurale della Regione Veneto Misura 124 DGR 745, 15 March 2010 «Cooperazione per lo sviluppo di nuovi prodotti, processi e tecnologie nel settore agricolo» project “PROBIOSER”.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Arne Janssen.
Rights and permissions
About this article
Cite this article
Pozzebon, A., Boaria, A. & Duso, C. Single and combined releases of biological control agents against canopy- and soil-dwelling stages of Frankliniella occidentalis in cyclamen. BioControl 60, 341–350 (2015). https://doi.org/10.1007/s10526-014-9641-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-014-9641-4