Abstract
Tuta absoluta Meyrick quickly developed into a significant pest of tomatoes worldwide. While the mirid bugs Macrolophus basicornis (Stal), Engytatus varians (Distant) and Campyloneuropsis infumatus (Carvalho) prey on this tomato borer, their biology have not been well characterized. Using a mixture of T. absoluta eggs and larvae as food on tomato, mirid life histories were studied. Nymphs and adults successfully used T. absoluta as prey, although significant differences in biology of the species were observed. Campyloneuropsis infumatus and M. basicornis were quickest and slowest to become adult at 16 and 19 days, respectively. Nymphal survival was high and varied from 70 to 75 %. Female biased sex ratios were observed for C. infumatus (0.80) and M. basicornis (0.71), but not for E. varians (0.56). Intrinsic rates of increase for C. infumatus, E. varians and M. basicornis were 0.11, 0.10 and 0.11 respectively. Our results indicate rapid development and population increase of these three mirids, making them interesting candidates for biological control of T. absoluta on tomato.
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References
Abbas S, Pérez-Hedo M, Colazza S, Urbaneja A (2014) The predatory mirid Dicyphus maroccanus as a new potential biological control agent in tomato crops. BioControl 59:565–574
Birch LC (1948) The intrinsic rate of natural increase of an insect population. J Anim Ecol 17:15–26
Bonato O, Couton L, Fargues J (2006) Feeding preference of Macrolophus caliginosus (Heteroptera: Miridae) on Bemisia tabaci and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). J Econ Entomol 99:1143–1151
Bueno VHP, van Lenteren JC (2012) Predatory bugs (Heteroptera). In: Panizzi AR, Parra JRP (eds) Insect bioecology and nutrition for integrated pest management. CRC Press, Boca Raton, pp 539–569
Bueno VHP, Montes FC, Calixto AM, Lins JC, van Lenteren JC (2012) Can recently found Brazilian hemipteran predatory bugs control Tuta absoluta? Integrated control in protected crops, Mediterranean climate. IOBC/WPRS Bulletin 80:63–67
Bueno VHP, van Lenteren JC, Lins JC Jr, Calixto AM, Montes FC, Silva DB, Santiago L, Pérez L (2013) New records of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) predation by Brazilian Hemipteran predatory bugs. J Appl Entomol 137:29–34
Calvo FJ, Bolckmans K, Belda JE (2011) Control of Bemisia tabaci and Frankliniella occidentalis in cucumber by Amblyseius swirskii. BioControl 56:185–192
Calvo FJ, Bolckmans K, Belda JE (2012) Release rate for a pre-plant application of Nesidiocoris tenuis for Bemisia tabaci control in tomato. BioControl 57:809–817
Castañé C, Iriarte J, Lucas E (2002) Comparison of prey consumption by Dicyphus tamaninii reared conventionally, and on a meat-based diet. BioControl 47:657–666
Castineiras A (1995) Natural enemies of Bemisia tabaci (Homoptera: Aleyrodidae) in Cuba. Fla Entomol 78:538–540
De Puysseleyr V, De Man S, Höfte M, De Clercq P (2012) Plantless rearing of the zoophytophagous bug Nesidiocoris tenuis. BioControl 58:205–213
Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Catalán Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, Urbaneja A (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215
Desneux N, Luna MG, Guillemaud T, Urbaneja A (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408
Ferreira PSF, Henry TJ (2011) Synopsis and keys to the tribes, genera, and species of Miridae (Hemiptera: Heteroptera) of Minas Gerais, Brazil Part I: Bryocorinae. Zoo 2920:1–41
Gillespie D, McGregor R (2000) The functions of plant feeding in the omnivorous predator Dicyphus hesperus: water places limits on predation. Ecol Entomol 25:380–386
Gontijo PC, Picanço MC, Pereira EJG, Martins JC, Chediak M, Guedes RNC (2013) Spatial and temporal variation in the control failure likelihood of the tomato leaf miner, Tuta absoluta. Ann Appl Biol 162:50–59
Hamdan A-JS (2006) Effect of host-plant species on the survival, adult longevity and fertility of predatory bug, Macrolophus caliginosus Wagner [Hemiptera: Miridae]. Hebron Univ Res J 2:1–15
Ingegno BL, Ferracini C, Gallinotti D, Alma A, Tavella L (2013) Evaluation of the effectiveness of Dicyphus errans (Wolff) as predator of Tuta absoluta (Meyrick). Biol Control 67:246–252
Lykouressis D, Perdikis D, Charalampous P (2014) Plant food effects on prey consumption by the omnivorous predator Macrolophus pygmaeus. Phytoparasitica 42:303–309
Mackauer M (1983) Quantitative assessment of Aphidius smithi (Hymenoptera: Aphidiidae): fecundity, intrinsic rate of increase, and functional response. Can Entomol 115:399–415
Maia AHN, Luiz AJ, Campanhola C (2000) Statistical inference on associated fertility life table parameters using jackknife technique: computational aspects. J Econ Entomol 93:511–518
Martínez AM, Baena M, Figueroa JI, Del Estal P, Medina M, Guzman-Lara E, Pineda S (2014) Primer registro de Engytatus varians (Distant) (Hemiptera: Heteroptera: Miridae) em México y su depredación sobre Bactericera cockerelli (Sulc) (Hemiptera:Triozidae): uma revisíon de su distribución y hábitos. Acta Zoológica Mexicana 30:617–624
Miranda MMM, Picanço MC, Zanuncio JC, Guedes RNC (1998) Ecological life table of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Bio Sci Tech 8:597–606
Mohamed E, Mahmoud M, Elhaj M, Mohamed S, Ekesi S (2015) Host plants record for tomato leaf miner Tuta absoluta (Meyrick) in Sudan. EPPO Bull 45:108–111
Mollá O, Biondi A, Alonso-Valiente M, Urbaneja A (2014) A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. BioControl 59:175–183
Montes FC (2013) Características biológicas dos estágios imaturos de três predadores (Hem.: Miridae) alimentados com ovos de Anagasta kuehniella (Zeller) (Lep.: Pyralidae) em cinco temperaturas. MSc. Thesis, Federal University of Lavras, Brazil
Nishikawa H, Shimada T, Nakahira K, Arakawa R (2010) Thermal effect on the development and reproduction of an indigenous mirid bug, Pilophorus typicus Distant (Heteroptera: Miridae), a potential biological control agent in Japan. Appl Entomol Zool 45:313–318
Perdikis D, Lykouressis D (2000) Effects of various items, host plants, and temperatures on the development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae). Biol Control 17:55–60
Pérez-Hedo M, Urbaneja A (2014) Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci 88:65–73
Pfeiffer D, Muniappan R, Sall D, Diatta P, Diongue A, Dieng E (2013) First record of Tuta absoluta (Lepidoptera: Gelechiidae) in Senegal. Fla Entomol 96:661–662
R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for statistical computing. R Development Core Team, Vienna
Rasdi ZM, Fauziah I, Wan Mohamad WAK (2009) Biology of Macrolophus caliginosus (Heteroptera: Miridae) predator of Trialeurodes vaporariorum (Homoptera: Aleyrodidae). Int J Biol 1:63–70
Sanchez JA (2008) Zoophytophagy in the plantbug Nesidiocoris tenuis. Agric For Entomol 10:75–80
SAS Institute (2009) JMP release 8: statistics and graphics guide. SAS Institute, Cary
Silva DB, Bueno VHP, Lins JC Jr, van Lenteren JC (2015) Life history data and population growth of Tuta absoluta at constant and alternating temperatures on two tomato lines. Bull Insectol 68(2):223–232
Silva DB, Bueno VHP, van Loon JJA, Penaflor MFGV, Bento JMS, van Lenteren JC (2016) Phloem-feeder Bemisia tabaci does not interfere with attaction of mirid predators to leaf-feeder Tuta absoluta infested tomato. (in preparation)
Tommasini MG, van Lenteren JC, Burgio G (2004) Biological traits and predation capacity of four Orius species on two prey species. Bull Insectol 57:79–94
Urbaneja A, Tapia G, Stansly P (2005) Influence of host plant and prey availability on developmental time and surviorship of Nesidiocoris tenius (Het.: Miridae). Biocontrol Sci Technol 15:513–518
Urbaneja A, González-Cabrera J, Arnó J, Gabarra R (2012) Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Manag Sci 68:1215–1222
van Lenteren JC (2010) Ecology: cool science, but does it help? Wageningen University, Wageningen
van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57:1–20
Vandekerkhove B, De Clercq P (2010) Pollen as an alternative or supplementary food for the mirid predator Macrolophus pygmaeus. Biol Control 53:238–242
Wheeler AG (2001) Biology of the plant bugs (Hemiptera: Miridae): pests, predators, opportunists. Cornell University Press, Ithaca
Acknowledgments
We thank Dr. Les Shipp (Canada) and two anonymous reviewers for correction of the manuscript, the Coordination for the Improvement of Higher Education Personnel (CAPES) (CAPES/NUFFIC Programme Project 044/12) and the National Council for Scientific and Technology Research (CNPq) for financial support of the project.
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Handling Editor: Marta Montserrat.
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Silva, D.B., Bueno, V.H.P., Montes, F.C. et al. Population growth of three mirid predatory bugs feeding on eggs and larvae of Tuta absoluta on tomato. BioControl 61, 545–553 (2016). https://doi.org/10.1007/s10526-016-9736-1
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DOI: https://doi.org/10.1007/s10526-016-9736-1