Assessment of Chrysoperla comanche (Banks) and Chrysoperla externa (Hagen) as Biological Control Agents of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) on Tomato (Solanum lycopersicum) under Glasshouse Conditions
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Production and Maintenance
2.2. The Insects
2.3. Bioassays
2.4. Statistical Analysis
3. Results
Consumption of Frankliniella occidentalis by First, Second and Third Instar of Chrysoperla comanche and Chrysoperla Externa on Tomato Plants
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- SIAP. Servicio de Información y Estadística Agroalimentaria y Pesquera. Producción Nacional de Tomate. 2017. Available online: http://infosiap.siap.gob.mx (accessed on 12 January 2017).
- FAO. FAOSTAT. Producción Mundial de Tomates en Fresco 2016. 2018. Available online: http://www.fao.org/faostat/es/#data/QC (accessed on 12 May 2018).
- Cloyd, R. Effects of Predators on the Belowground Life Stages (Prepupae and Pupae) of the Western Flower Thrips, Frankliniella occidentalis (Thripidae: Thysanoptera): A Review. Adv. Entomol. 2019, 7, 71–80. [Google Scholar] [CrossRef] [Green Version]
- Webster, C.; Reitz, S.R.; Perry, K.; Adkins, S. A natural M RNA reassortant arising from two species of plant -and insect-infecting bunyaviruses and comparison of its sequence and biological properties to parental species. Virology 2011, 413, 215–225. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gilbertson, R.L.; Batuman, O.; Webster, G.; Adkins, S. Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Annu. Rev. Virol. 2015, 2, 67–93. [Google Scholar] [CrossRef] [PubMed]
- Ramírez, R.S.; Osuna, C.F.J.; Vázquez, A.J.M.P.; Bustamante, O.J.D.; Canul, K.J.; Ocampo, O.T. Plagas y Enfermedades del Jitomate Cultivado en Invernaderos y Bioespacios del Estado de Morelos; Folleto Técnico No. 37; Campo Experimental Zacatepec, INIFAP: Zacatepec, México, 2009; p. 77. [Google Scholar]
- Inmaraju, J.A.; Paine, T.D.; Bethke, J.A.; Roob, K.L.; Newman, J.P. Western flower thrips (Thysanoptera: Thripidae) resistance to insecticides in coastal California greenhouses. J. Econ. Entomol. 1992, 85, 9–14. [Google Scholar] [CrossRef]
- Brøadsgaard, H.F. Insecticide resistance in European and African strains of western flower thrips (Thysanoptera: Thripidae) tested in a new residue-on-glass test. J. Econ. Entomol. 1994, 87, 1141–1146. [Google Scholar] [CrossRef]
- Broadbent, A.B.; Pree, D.J. Resistance to insecticides in populations of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) from greenhouses in the Niagara Region of Ontario. Can. Entomol. 1997, 129, 907–913. [Google Scholar] [CrossRef]
- Espinosa, P.J.; Bielza, P.; Contreras, J.; Lacasa, A. Insecticide resistance in field populations of Frankliniella occidentalis (Pergande) in Murcia (south-east Spain). Pest Manag. Sci. 2002, 58, 967–971. [Google Scholar] [CrossRef]
- Nuez, F. El Cultivo del Tomate.; Mundi-Prensa: Madrid, España, 1995; p. 796. [Google Scholar]
- Bianchi, F.J.; Ives, A.R.; Schellhorn, N.A. Interactions between conventional and organic farming for biocontrol services across the landscape. Ecol. Appl. 2013, 23, 1531–1543. [Google Scholar] [CrossRef]
- Perdikis, D.; Kapaxidi, E.; Papadoulis, G. Biological control of insect and mite pests in greenhouse solanaceous crops. Eur. J. Plant Sci. Biotechnol. 2008, 2, 125–144. [Google Scholar]
- Chow, A.; Chau, A.; Heinz, K.M. 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. 2010, 53, 188–196. [Google Scholar] [CrossRef]
- Xu, X.N.; Borgemeister, C.; Poehling, H.M. Biocontrol of wester flower thrips Frankliniella occidentalis (Pergande) by combined releases of plant-inhabiting predatory mite, Amblyseius cucumeris Oudemans or bug, Orius insidious Say with Soil-dwelling mite, Hypoaspis Aculeifer Canestrini. China Agric. Sci. Technol. Press 2005, 35–40. [Google Scholar]
- Luna, E.H.M.; Canizal, M.A.; Luna, E.J.C.; Castrejón, G.V.R. Comportamiento de búsqueda y capacidad depredadora de Chrysoperla externa sobre Frankliniella occidentalis. South Entomol. 2017, 42, 463–476. [Google Scholar]
- Salamanca, J.; Varón, E.; Santos, O. Cría y evaluación de la capacidad de depredación de Chrysoperla externa sobre Neohydatothrips signifer, thrips plaga del cultivo de maracuyá. Cienc. Tecnol. Agropec. 2010, 11, 31–40. [Google Scholar]
- Rodrigues, C.A.; Battel, A.P.M.B.; Martinelli, N.M.; Moral, R.D.A.; Sercundes, R.K.; Godoy, W.A.C. Dynamics and predation efficiency of Chrysoperla externa (Neuroptera: Chrysopidae) on Enneothrips flavens (Thysanoptera: Thripidae). Fla. Entomol. 2014, 97, 653–659. [Google Scholar] [CrossRef]
- Moraes, C.J.; Goussain, M.M.; Basagli, A.B.M.; Carvalho, A.G.; Carvalho, E.C.; Sampaio, V.M. Silicon influence on the tritrophic interaction: Wheat plants, the greenbug Schizaphis graminum (Rondani) (Hemiptera: Aphididae), and its natural enemies, Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae) and Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Neotrop. Entomol. 2004, 33, 619–624. [Google Scholar]
- Barbosa, L.R.; Carvalho, C.F.; Souza, B.; Auad, A.M. Influência da densidade de Myzus persicae (Sulzer) sobre algunos aspectos biológicos e capacidade predatória de Chrysoperla externa (Hagen). Acta Sci. Agron. 2006, 28, 227–231. [Google Scholar] [CrossRef]
- Flores, G.C.; Reguilón, C.; Alderete, L.G.; Kirschbaum, D.S. Liberación de Chrysoperla argentina (Neuroptera: Chrysopidae) para el control de Trialeurodes vaporariorum (Westwood) (Hemiptera, Aleyrodidae) en invernáculo de pimiento en Tucumán, Argentina. Intropica 2015, 10, 28–36. [Google Scholar] [CrossRef]
- Cortez, M.E.; López, A.J.I.; Rodríguez, L.; Partida, V.M.P.; Pérez, M.J. Especies de Chrysopidae asociadas a Diaphorina citri Kuwayama en cítricos y capacidad de depredación en Sinaloa, México. Rev. Mex. Cienc. Agric. 2016, 7, 363–374. [Google Scholar]
- Bonneau, P.; Renkema, J.; Fournier, V.; Firlej, A. Ability of Muscidifurax raptorellus and other parasitoids and predators to control Drosophila suzukii populations in raspberries in the laboratory. Insects 2019, 10, 68. [Google Scholar] [CrossRef] [Green Version]
- Tulisalo, U. Biological Control in the Greenhouse. In Biology of Chrysopidae; Canard, M., Séméria, Y., New, T.R., Eds.; Dr. W. Junk: The Hague, The Netherlands, 1984; pp. 228–233. [Google Scholar]
- Shrestha, G.; Enkegaard, A. The green lacewing, Chrysoperla carnea: Preference between lettuce aphids, Nasonovia ribisnigri, and western flower thrips, Frankliniella occidentalis. J. Insect Sci. 2013, 13, 94. Available online: http://www.insectscience.org/13.94 (accessed on 19 November 2019).
- Breene, R.G.; Meagher, R.L., Jr.; Nordlund, D.A.; Yin-Tung, W. Biological control of Bemisia tabaci (Homoptera: Aleyrodidae) in a greenhouse using Chrysoperla rufilabris (Neuroptera: Chrysopidae). Biol. Control 1992, 2, 9–14. [Google Scholar]
- Sarkar, S.C.; Wang, E.; Zhang, Z.; Wu, S.; Lei1, Z. Laboratory and glasshouse evaluation of the green lacewing, Chrysopa pallens (Neuroptera: Chrysopidae) against the western fower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae). Appl. Entomol. Zool. 2019, 54, 115–121. [Google Scholar] [CrossRef]
- Hoddle, M.S.; Mound, L.A.; Paris, D.L. Thrips of California; CBIT Publishing: Brisbane, Queensland, Australia, 2012; Available online: http://Keys.lucidcentral.Org/keys/v3/thrips_of_california/Thrips_of_california.hml. (accessed on 25 January 2017).
- Brooks, S.J.; Barnard, P.C. The green lacewings of the world: A generic review (Neuroptera: Chrysopidae). Bull. Br. Mus. Nat. Hist. Entomol. 1990, 59, 117–286. [Google Scholar]
- Vogt, H.; Viñuela, E.; Bozsik, A.; Hilbeck, A.; Bigler, F. Interactions with plant management strategies. In Lacewings in the Crop Environment; McEwen, P., New, T.R., Wihittingogt, A.E., Eds.; Cambridge University Press: Cambridge, UK, 2000; pp. 357–379. [Google Scholar]
- Auad, A.M.; De Freitas, S.; Barbosa, L.R. Influencia de la dieta en la respuesta funcional de Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae) alimentadas con Uroleucon ambrosiae (Thomas) (Hemíptera: Aphididae). Bol. San. Veg. Plagas. 2001, 27, 455–463. [Google Scholar]
- Schneider, M.I.; Sánchez, N.; Pineda, S.; Chi, H.; Ronco, A. Impact of glyphosate on the development, fertility and demography of Chrysoperla externa (Neuroptera: Chrysopidae): Ecological approach. Chemosphere 2009, 76, 1451–1455. [Google Scholar] [CrossRef] [PubMed]
- Ail-Catzim, C.; Flores-Dávila, M.; Cerna-Chávez, E.; Badii-Zabeh, M.; Landeros-Flores, J.; Ochoa-Fuentes, Y.; Aguirre-Uribe, L. Respuesta funcional de diferentes instares larvales de Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) sobre ninfas de Bactericera cockerelli (Sulc) (Homoptera: Psyllidae). Rev. Fac. Cienc. Agrar. 2012, 44, 279–288. [Google Scholar]
- Castro, L.M.A.; Martínez, O.J.W.; Dotor, R.M.Y. Evaluación del efecto regulador de Chrysoperla externa sobre mosca blanca Trialeurodes vaporariorum en tomate. Rev. Cienc. Agríc. 2016, 33, 43–54. [Google Scholar] [CrossRef] [Green Version]
- Toscano, L.C.; Auad, A.M.; Figueira, L.K. Comportamiento de Chrysoperla externa (Hagen, 1861) em genotipos de tomateiiro infestados com ovos de Bemisia tabaci (Genadius, 1889) biotipo B em laboratorio. Arq. Inst. Biol. 2003, 70, 117–121. [Google Scholar]
- Turcios, P.L.A.; Bautista, M.N.; Johansen, N.R.; Romero, N.J.; Segura, L.O.; Sánchez, A.H.; Vera, G.J. Population fluctuations of thrips (Thysanoptera) and their relationship to the phenology of vegetable crops in the central region of Mexico. Fla. Entomol. 2015, 98, 430–438. [Google Scholar]
- Barbosa, L.R.; Auad, A.M.; Freitas, S. Capacidade predatória de Chrysoperla externa alimentada com Frankliniella schultzei em plantas de alface de cultivo hidropônico. Rev. Agric. 2000, 75, 349–358. [Google Scholar]
- Aguirre, L.A.; Miranda, M.A.; Urías, L.M.A.; Orona, F.; Almeyda, L.I.H.; Johansen, N.R.; Tucuch, M. Especies de thrips (Thysanoptera) en mango, fluctuación y abundancia. Rev. Colomb. Entomol. 2013, 39, 9–12. [Google Scholar]
- Mujica, M.V.; Scantoni, I.B.; Franco, J.; Nuñez, S.; Bentancourt, C.M. Fluctuación poblacional de Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) en Vitis vinífera L. cv. Italia en la zona sur de Uruguay. Bol. San. Veg. Plagas 2007, 33, 457–467. [Google Scholar]
- Santos, A.O.; Varón, D.E.H.; Gaigl, A.; Floriano, A. Nivel de daño económico para Neohydatothrips signifer (Thysanoptera: Thripidae) en maracuyá en el Huila, Colombia. Rev. Colomb. Entomol. 2012, 38, 23–29. [Google Scholar]
- Granadillo, J. Integrated Pest Management of Western Flower Thrips; Universiteit Utrecht: Utrecht, The Netherlands, 2014; p. 32. [Google Scholar]
- Elimem, M.; Teixeira da Silva, J.A.; Chermiti, B. Double-attraction method to control Frankliniella occidentalis (Pergande) in pepper crops in Tunisia. Plant. Prot. Sci. 2014, 50, 90–96. [Google Scholar] [CrossRef] [Green Version]
- Jan de Kogel, W.; van Deventer, P. Intraspecific attraction in the western flower thrips, Frankliniella occidentalis; indications for a male sex pheromone. Entomol. Exp. Appl. 2003, 107, 87–89. [Google Scholar] [CrossRef] [Green Version]
- Kirk, W.D.J. The aggregation pheromones of thrips (Thysanoptera) and their potential for pest management. Int. J. Trop. Insect Sci. 2017, 37, 41–49. [Google Scholar] [CrossRef] [Green Version]
- Shuang-Shuang, G.; Xiao-Wei, L.; Jin-Ming, Z.; Zhi-Jun, Z.; Yao-Bin, L. Field testing of aggregation pheromones of Frankliniella occidentalis and F. intonsa (Thysanoptera: Thripidae) and their roles in interspecific interaction. Acta Entomol. Sin. 2017, 60, 1447–1456. [Google Scholar]
- Covaci, A.D.; Oltean, I.; Pop, A. Evaluation of Pheromone Lure as Mass-Trapping Tools for Western Flower Thrips. Bull. UASVM Agric. 2012, 69, 333–334. [Google Scholar]
- Plouvier, W.N.; Wajnberg, E. Improving the efficiency of augmentative biological control with arthropod natural enemies: A modeling approach. Biol. Control 2018, 125, 121–130. [Google Scholar] [CrossRef]
Species | Vegetative Stage X2 = 0.632, df = 2, p > 0.05 | Blooming Stage X2 = 1.686, df = 2, p > 0.05 | Total | ||||||
---|---|---|---|---|---|---|---|---|---|
L1 | L2 | L3 | Total | L1 | L2 | L3 | Total | ||
C. comanche | 19 | 29 | 30 | 78 | 20 | 113 | 125 | 258 | 336 |
C. externa | 26 | 34 | 30 | 90 | 31 | 118 | 148 | 297 | 387 |
Total | 45 | 63 | 60 | 168 | 51 | 231 | 273 | 555 | 723 |
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Luna-Espino, H.M.; Jiménez-Pérez, A.; Castrejón-Gómez, V.R. Assessment of Chrysoperla comanche (Banks) and Chrysoperla externa (Hagen) as Biological Control Agents of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) on Tomato (Solanum lycopersicum) under Glasshouse Conditions. Insects 2020, 11, 87. https://doi.org/10.3390/insects11020087
Luna-Espino HM, Jiménez-Pérez A, Castrejón-Gómez VR. Assessment of Chrysoperla comanche (Banks) and Chrysoperla externa (Hagen) as Biological Control Agents of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) on Tomato (Solanum lycopersicum) under Glasshouse Conditions. Insects. 2020; 11(2):87. https://doi.org/10.3390/insects11020087
Chicago/Turabian StyleLuna-Espino, Héctor Manuel, Alfredo Jiménez-Pérez, and Víctor Rogelio Castrejón-Gómez. 2020. "Assessment of Chrysoperla comanche (Banks) and Chrysoperla externa (Hagen) as Biological Control Agents of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) on Tomato (Solanum lycopersicum) under Glasshouse Conditions" Insects 11, no. 2: 87. https://doi.org/10.3390/insects11020087
APA StyleLuna-Espino, H. M., Jiménez-Pérez, A., & Castrejón-Gómez, V. R. (2020). Assessment of Chrysoperla comanche (Banks) and Chrysoperla externa (Hagen) as Biological Control Agents of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) on Tomato (Solanum lycopersicum) under Glasshouse Conditions. Insects, 11(2), 87. https://doi.org/10.3390/insects11020087