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Attraction and Oviposition of Tuta absoluta Females in Response to Tomato Leaf Volatiles

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Abstract

The tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae) is a devastating pest of cultivated tomato Solanum lycopersicum throughout South and Central America and Europe. We aimed to characterize the behavioral mechanisms and the chemical cues involved in host selection of T. absoluta females by chemical analysis of tomato leaf volatiles, wind tunnel attraction assays, and oviposition bioassays. Tomato leaf odor elicited in mated females upwind orientation flight followed by landing as well as egg-laying, demonstrating the essential role of plant volatiles in T. absoluta host-finding behavior. In wind tunnel and oviposition choice experiments, T. absoluta females significantly preferred tomato S. lycopersicum over wild tomato Solanum habrochaites, which is resistant to larval feeding. This indicates that leaf volatiles provide information on the suitability of plants as larval hosts. Mated females also discriminated three cultivars of S. lycopersicum according to their volatile profiles. Headspace collections from leaves of these three cultivars contained large amounts of β-phellandrene, followed by limonene, 2-carene, and (E)-β-caryophyllene, which together accounted for more than 70% of tomato foliage headspace. Most leaf volatiles were released by all three cultivars, but they showed significant differences with respect to the presence of a few minor compounds and blend proportion. This is an initial study of the volatile signatures that mediate attraction and oviposition of tomato leafminer T. absoluta in response to its main host, tomato.

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References

  • Arab, A., Trigo, J. R., Lourenção, A. L., Peixoto, A. M., Ramos, F., and Bento, J. M. S. 2007. Differential attractiveness of potato tuber volatiles to Phthorimaea operculella (Gelechiidae) and the predator Orius insidiosus (Anthocoridae). J. Chem. Ecol. 33:1845–1855.

    Article  PubMed  CAS  Google Scholar 

  • Azevedo, S.M., Faria, M.V., Maluf, W.R., De Oliveira, A.C.B., and De Freitas, J.A. 2003. Zingiberene-mediated resistance to the South American tomato pinworm derived from Lycopersicon hirsutum var. hirsutum. Euphytica 134:347–351.

    Article  Google Scholar 

  • Bengtsson, M., Backman, A. C., Liblikas, I., Ramirez, M. I., Borg-Karlson, A. K., Ansebo, L., Anderson, P., Lofqvist, J., and Witzgall, P. 2001. Plant odor analysis of apple: antennal response of codling moth females to apple volatiles during phenological development. J. Agric. Food Chem. 49:3736–3741.

    Article  PubMed  CAS  Google Scholar 

  • Bengtsson, M., Jaastad, G., Knudsen, G., Kobro, S., Backman, A. C., Pettersson, E., and Witzgall, P. 2006. Plant volatiles mediate attraction to host and non-host plant in apple fruit moth, Argyresthia conjugella. Entomol. Exp. Appl. 118:77–85.

    Article  CAS  Google Scholar 

  • Bleeker, P. M., Diergaarde, P. J., Ament, K., Guerra, J., Weidner, M., Schutz, S., De Both, M. T. J., Haring, M. A., and Schuurink, R. C. 2009. The role of specific tomato volatiles in tomato-whitefly interaction. Plant Physiol. 151:925–935.

    Article  PubMed  CAS  Google Scholar 

  • Bleeker, P. M., Diergaarde, P., Ament, K., Schütz, S., Johne, B., Dijkink, J., Hiemstra, H., de Gelder, R., de Both, M. T. J., Sabelis, M. W., Haring, M. A., and Schuurink, R. C. 2011. Tomato-produced 7-epizingiberene and R-curcumene act as repellents to whiteflies. Phytochemistry 72:68–73.

    Article  PubMed  CAS  Google Scholar 

  • Bogorni, P. C., Silva, R. A., and Carvalho G. S. 2003. Leaf mesophyll consumption by Tuta absoluta (Meyrick, 1971) in three cultivars of Lycopersicon esculentum Mill. Cienc. Rural 33:7–11.

    Article  Google Scholar 

  • Bray, J. R. and Curtis, J. T. 1957. An ordination of the upland forest communities of Southern Wisconsin. Ecol. Monogr. 27:326–349.

    Article  Google Scholar 

  • Buttery, R. G., Ling, L. C., and Light, D. M. 1987. Tomato leaf volatile aroma components. J. Agric. Food Chem. 35:1039–1042.

    Article  CAS  Google Scholar 

  • Calatayud, P. A., Guenego, H., Ahuya, P., Wanjoya, A., Ru, B. L., Silvain, J. F., and Frerot, B. 2008. Flight and oviposition behaviour of the African stem borer, Busseola fusca, on various host plant species. Entomol. Exp. Appl. 129:348–355.

    Article  Google Scholar 

  • Cha, D. H., Nojima, S., Hesler, S. P., Zhang, A., Linn, C. E., Roelofs, W. L., and Loeb, G. M. 2008. Identification and field evaluation of grape shoot volatiles attractive to female grape berry moth (Paralobesia viteana). J. Chem. Ecol. 34:1180–1189.

    Article  PubMed  CAS  Google Scholar 

  • Crawley, M. J. C. 2005. The R Book. Wiley, Chichester.

    Google Scholar 

  • Degenhardt, J., Kollner, T. G., and Gershenzon, J. 2009. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621–1637.

    Article  PubMed  CAS  Google Scholar 

  • Desneux, N., Wajnberg, E., Wyckhuys, K. A. G., Burgio, G., Arpaia, S., Narvaez-Vasquez, C. A., Gonzalez-Cabrera, J., Ruescas, D. C., Tabone, E., Frandon, J., Pizzol, J., Poncet, C., Cabello, T., and 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.

    Article  Google Scholar 

  • Dudareva, N., Pichersky, E., and Gershenzon, J. 2004. Biochemistry of plant volatiles. Plant Physiol. 135:1893–1902.

    Article  PubMed  CAS  Google Scholar 

  • Dufrêne, M. and Legendre, P. 1997. Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecol. Monogr. 67:345–366.

    Google Scholar 

  • Eigenbrode, S. D., Trumble, J. T., Millar, J. G., and White, K. K. 1994. Topical toxicity of tomato sesquiterpenes to the beet armyworm and the role of these compounds in resistance derived from an accession of Lycopersicon hirsutum f. typicum. J. Agric. Food Chem. 42:807–810.

    Article  CAS  Google Scholar 

  • Fenemore, P. G. 1988. Host-plant location and selection by adult potato moth, Phthorimaea operculella (Lepidoptera, Gelechiidae) - a review. J. Insect Physiol. 34:175–177.

    Article  Google Scholar 

  • Fraser, A. M., Mechaber, W. L., and Hildebrand, J. G. 2003. Electroantennographic and behavioral responses of the sphinx moth Manduca sexta to host plant headspace volatiles. J. Chem. Ecol. 29:1813–1833.

    Article  PubMed  CAS  Google Scholar 

  • Horgan, F. G., Quiring, D. T., Lagnaoui, A., and Pelletier, Y. 2007. Variable responses of tuber moth to the leaf trichomes of wild potatoes. Entomol. Exper. Appl. 125:1–12.

    Article  Google Scholar 

  • Kang, J. H., Liu, G. H., Shi, F., Jones, A. D., Beaudry, R. M., and Howe, G. A. 2010. The tomato odorless-2 mutant is defective in trichome-based production of diverse specialized metabolites and broad-spectrum resistance to insect herbivores. Plant Physiol. 154:262–272.

    Article  PubMed  CAS  Google Scholar 

  • Karlsson, M. F., Birgersson, G., Prado, A. M. C., Bosa, F., Bengtsson, M., and Witzgall, P. 2009. Plant odor analysis of potato: response of Guatemalan moth to above- and belowground potato volatiles. J. Agric. Food Chem. 57:5903–5909.

    Article  PubMed  CAS  Google Scholar 

  • Kennedy, G. G. 2003. Tomato, pests, parasitoids, and predators: Tritrophic interactions involving the genus Lycopersicon. Annu. Rev. Entomol. 48:51–72.

    Article  PubMed  CAS  Google Scholar 

  • Knudsen, J. T., Eriksson, R., Gershenzon, J., and Ståhl, B. 2006. Diversity and distribution of floral scent. Bot. Rev. 72:1–120.

    Article  Google Scholar 

  • Knudsen, G. K., Bengtsson, M., Kobro, S., Jaastad, G., Hofsvang, T., and Witzgall, P. 2008. Discrepancy in laboratory and field attraction of apple fruit moth Argyresthia conjugella to host plant volatiles. Physiol. Entomol. 33:1–6.

    Article  CAS  Google Scholar 

  • Leite, G. L. D., Picanco, M., Della, L., and Moreira, M. D. 1999. Role of canopy height in the resistance of Lycopersicon hirsutum f. glabratum to Tuta absoluta (Lep.; Gelechiidae). J. Appl. Entomol. 123:459–463.

    Article  Google Scholar 

  • Leite, G. L. D., Picanco, M., Guedes, R. N. C., and Zanuncio, J. C. 2001. Role of plant age in the resistance of Lycopersicon hirsutum f. glabratum to the tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae). Sc. Hortic. 89:103–113.

    Article  Google Scholar 

  • Lietti, M. M. M., Botto, E., and Alzogaray, R. A. 2005. Insecticide resistance in Argentine populations of Tuta absoluta (Meyrick) (Lepidoptera : Gelechiidae). Neotrop. Entomol. 34:113–119.

    Article  Google Scholar 

  • Linn, C. E., Feder, J. L., Nojima, S., Dambroski, H. R., Berlocher, S. H., and Roelofs, W. L. 2003. Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proc. Natl. Acad. Sci. USA 100:11490–11493.

    Article  PubMed  CAS  Google Scholar 

  • Masante-Roca, I., Anton, S., Delbac, L., Dufour, M. C., and Gadenne, C. 2007. Attraction of the grapevine moth to host and non-host plant parts in the wind tunnel: effects of plant phenology, sex, and mating status. Entomol. Exp. Appl. 122:239–245.

    Article  Google Scholar 

  • McArdle, B. H. and Anderson, M. J. 2001. Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology 82:290–297.

    Article  Google Scholar 

  • Najar-Rodriguez, A. J., Galizia, C. G., Stierle, J., and Dorn, S. 2010. Behavioral and neurophysiological responses of an insect to changing ratios of constituents in host plant-derived volatile mixtures. J. Exp. Biol. 213:3388–3397.

    Article  PubMed  CAS  Google Scholar 

  • Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Gavin, L., Simpson, G. L., and Stevens, M.H.H. 2008. Vegan: community ecology package. R package version 1.11-4. http://cran.r-project.org/, http://vegan.r-forge.r-project.org/.

  • Oliveira, F. A., Da Silva, D. J. H., Leite, G. L. D., Jham, G. N., and Picanco, M. 2009. Resistance of 57 greenhouse-grown accessions of Lycopersicon esculentum and three cultivars to Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Scientia Horticulturae 119:182–187.

    Article  CAS  Google Scholar 

  • Pichersky, E., Sharkey, T. D., and Gershenzon, J. 2006. Plant volatiles: a lack of function or a lack of knowledge? Tr. Plant Sci. 11:421–421.

    Article  CAS  Google Scholar 

  • Pinero, J. C. and Dorn, S. 2009. Response of female oriental fruit moth to volatiles from apple and peach trees at three phenological stages. Entomol. Exp. Appl. 131:67–74.

    Article  Google Scholar 

  • Pontes, W. J. T., Lima, E. R., Cunha, E. G., De Andrade, P. M. T., Lobo, A. P., and Barros, R. 2010. Physical and chemical cues affect oviposition by Neoleucinodes elegantalis. Physiol. Entomol. 35:134–139.

    Article  Google Scholar 

  • Proffit, M., Chen, C., Soler, C., Bessiere, J. M., Schatz, B., and Hossaert-Mckey, M. 2009. Can chemical signals, responsible for mutualistic partner encounter, promote the specific exploitation of nursery pollination mutualisms? The case of figs and fig wasps. Entomol. Exp. Appl. 131:46–57.

    Article  CAS  Google Scholar 

  • Renwick, J. A. A. and Chew, F. S. 1994. Oviposition behavior in Lepidoptera. Annu. Rev. Entomol. 39:377–400.

    Article  Google Scholar 

  • Roberts, D. W. 2010. Laboratory for dynamic synthetic vegephenonenology (LabDSV) version 1.4-1. http://ecology.msu.montana.edu/labdsv/R

  • Sacchettini, J. C. and Poulter, C. D. 1997. Biochemistry - Creating isoprenoid diversity. Science 277:1788–1789.

    Article  PubMed  CAS  Google Scholar 

  • Salas, J. 2004. Capture of Tuta absoluta (Lepidoptera: Gelechiidae) in traps baited with its sex pheromone. Rev. Colomb. Entomol. 30:75–78.

    CAS  Google Scholar 

  • Schmidt-Busser, D., von Arx, M., and Guerin, P. M. 2009. Host plant volatiles serve to increase the response of male European grape berry moths, Eupoecilia ambiguella, to their sex pheromone. J. Comp. Physiol. A 195:853–864.

    Article  Google Scholar 

  • Siqueira, H. A. A., Guedes, R. N. C., and Picanco, M. C. 2000. Insecticide resistance in populations of Tuta absoluta (Lepidoptera: Gelechiidae). Agricult. Forest Entomol. 2:147–153.

    Article  Google Scholar 

  • Smith, R. M., Marshall, J. A., Davey, M. R., Lowe, K. C., and Power, J. B. 1996. Comparison of volatiles and waxes in leaves of genetically engineered tomatoes. Phytochemistry 43:753–758.

    Article  CAS  Google Scholar 

  • Sole, J., Sans, A., Riba, M., and Guerrero, A. 2010. Behavioural and electrophysiological responses of the European corn borer Ostrinia nubilalis to host-plant volatiles and related chemicals. Physiol. Entomol. 35:354–363.

    Article  CAS  Google Scholar 

  • Szendrei, Z. and Rodriguez-Saona, C. 2010. A meta-analysis of insect pest behavioral manipulation with plant volatiles. Entomol. Exp. Appl. 134:201–210.

    Article  Google Scholar 

  • Tasin, M., Backman, A. C., Bengtsson, M., Ioriatti, C., and Witzgall, P. 2006. Essential host plant cues in the grapevine moth. Naturwissenschaften 93:141–144.

    Article  PubMed  CAS  Google Scholar 

  • Tasin, M., Bäckman, A.-C., Coracini, M., Casado, D., Ioriatti, C., and Witzgall, P. 2007. Synergism and redundancy in a plant volatile blend attracting grapevine moth females. Phytochemistry 68:203–209.

    Article  PubMed  CAS  Google Scholar 

  • Tasin, M., Bäckman, A.-C., Anfora, G., Carlin, S., Ioriatti, C., and Witzgall, P. 2010. Attraction of female grapevine moth to common and specific olfactory cues from 2 host plants. Chem. Senses 35:57–64.

    Article  PubMed  Google Scholar 

  • Thompson, J. N. and Pellmyr, O. 1991. Evolution of oviposition behavior and host preference in Lepidoptera. Annu. Rev. Entomol. 36:65–89.

    Article  Google Scholar 

  • Torres, J. B., Faria, C. A., Evangelista, W. S., and Pratissoli, D. 2001. Within-plant distribution of the leaf miner Tuta absoluta (Meyrick) immatures in processing tomatoes, with notes on plant phenology. Int. J. Pest Manag. 47:173–178.

    Article  Google Scholar 

  • Vallat, A., and Dorn, S. 2005. Changes in volatile emissions from apple trees and associated response of adult female codling moths over the fruit-growing season. J. Agric. Food Chem. 53:4083–4090.

    Article  PubMed  CAS  Google Scholar 

  • Van der Hoeven, R. S., Monforte, A. J., Breeden, D., Tanksley, S. D., and Steffens, J. C. 2000. Genetic control and evolution of sesquiterpene biosynthesis in Lycopersicon esculentum and L. hirsutum. Plant Cell 12:2283–2294.

    Article  Google Scholar 

  • Witzgall, P., Kirsch, P., and Cork, A. 2010. Sex pheromones and their impact on pest management. J. Chem. Ecol. 36:80–100.

    Article  PubMed  CAS  Google Scholar 

  • Yan, F. M., Bengtsson, M., and Witzgall, P. 1999. Behavioral response of female codling moths, Cydia pomonella, to apple volatiles. J. Chem. Ecol. 25:1343–1351.

    Article  CAS  Google Scholar 

  • Zhang, P. Y., Chen, K. S., He, P. Q., Liu, S. H., and Jiang, W. F. 2008. Effects of crop development on the emission of volatiles in leaves of Lycopersicon esculentum and its inhibitory activity to Botrytis cinerea and Fusarium oxysporum. J. Integr. Plant Biol. 50:84–91.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This study was supported by the Swedish University of Agricultural Sciences (SLU) and by the Swedish Foundation for International Cooperation in Research and Higher Education (STINT) and EL was supported by FAPEMIG.

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Authors and Affiliations

  1. Chemical Ecology Group, Swedish University of Agricultural Sciences, 230 53, Alnarp, Sweden

    Magali Proffit, Göran Birgersson, Marie Bengtsson & Peter Witzgall

  2. UNIMONTES, Campus Universitário Prof. Darcy Ribeiro, Prédio 6 (CCBS)—Sala 200, Vila Mauricéia, Montes Claros, MG, 39401–089, Brazil

    Ronaldo Reis Jr.

  3. Departamento de Biologia Animal, Universidade Federal de Viçosa, Entomologia, Viçosa, MG, 36570–000, Brazil

    Eraldo Lima

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  1. Magali Proffit
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  2. Göran Birgersson
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Correspondence to Magali Proffit.

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Proffit, M., Birgersson, G., Bengtsson, M. et al. Attraction and Oviposition of Tuta absoluta Females in Response to Tomato Leaf Volatiles. J Chem Ecol 37, 565–574 (2011). https://doi.org/10.1007/s10886-011-9961-0

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