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Volatiles mediate host-selection in the corn hoppers Dalbulus maidis (Hemiptera: Cicadellidae) and Peregrinus maidis (Hemiptera: Delphacidae)

Published online by Cambridge University Press:  08 February 2019

M.V. Coll Aráoz Open the ORCID record for M.V. Coll Aráoz [Opens in a new window] ,
V.G. Jacobi Open the ORCID record for V.G. Jacobi [Opens in a new window] ,
P.C. Fernandez Open the ORCID record for P.C. Fernandez [Opens in a new window] ,
E. Luft Albarracin Open the ORCID record for E. Luft Albarracin [Opens in a new window] ,
E.G. Virla Open the ORCID record for E.G. Virla [Opens in a new window] ,
J.G. Hill Open the ORCID record for J.G. Hill [Opens in a new window]  and
C.A.N. Catalán Open the ORCID record for C.A.N. Catalán [Opens in a new window]
M.V. Coll Aráoz*
Affiliation:
PROIMI-Biotecnología, CONICET, Av. Belgrano y Pje. Caseros, S.M. de Tucumán, Tucumán, Argentina Facultad de Ciencias Naturales e IML, UNT, Miguel Lillo 205, San Miguel de Tucumán, Argentina
V.G. Jacobi
Affiliation:
INBA-CONICET, Instituto de Investigaciones en Biociencias Agrícolas y Ambientales, Buenos Aires, Argentina Facultad de Agronomía, Cátedras de Química de Biomoléculas y Genética, UBA, Av. San Martín 4453, CABA, Argentina
P.C. Fernandez
Affiliation:
Facultad de Agronomía, Cátedras de Química de Biomoléculas y Genética, UBA, Av. San Martín 4453, CABA, Argentina CONICET-INTA, EEA Delta del Paraná, Paraná de las Palmas y Cl Comas, Campana, Argentina
E. Luft Albarracin
Affiliation:
PROIMI-Biotecnología, CONICET, Av. Belgrano y Pje. Caseros, S.M. de Tucumán, Tucumán, Argentina
E.G. Virla
Affiliation:
PROIMI-Biotecnología, CONICET, Av. Belgrano y Pje. Caseros, S.M. de Tucumán, Tucumán, Argentina Instituto de Entomología, FM Lillo, Miguel Lillo 251, San Miguel de Tucumán, Argentina
J.G. Hill
Affiliation:
PROIMI-Biotecnología, CONICET, Av. Belgrano y Pje. Caseros, S.M. de Tucumán, Tucumán, Argentina
C.A.N. Catalán
Affiliation:
INQUINOA-CONICET, Instituto de Química Orgánica, Facultad de Bioquímica Química y Farmacia, Universidad Nacional de Tucumán, Ayacucho 491, San Miguel de Tucumán, Argentina
*
*Author for correspondence Phone: +54 381 434 4888 Fax: +54 381 434 4887 E-mail: victoriacoll@hotmail.com
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Abstract

Volatile organic compounds (VOCs) released by plants are generally involved in host recognition and host selection for many phytophagous insects. However, for leafhoppers and planthoppers, host recognition is mainly thought to involve a phototactic response, but it is not clear if a host plant could be selected based on the volatile cues it emits. In this study we evaluated olfactory responses in dual choice tests of two Hemiptera species, Dalbulus maidis (De Long) (Cicadellidae) and Peregrinus maidis (Ashmead) (Delphacidae), vectors of maize-stunting diseases, to three maize (Zea mays L.) germplasms, a temperate and a tropical hybrid and a landrace. VOCs emitted by the germplasms were collected and identified using gas chromatography-mass spectrometry. The temperate hybrid released significantly more VOCs than the tropical hybrid and the landrace, and its volatile profile was dominated by (±)-linalool. D. maidis preferred odours emitted from the temperate hybrid, whereas P. maidis preferred odours from the tropical hybrid and the landrace over the temperate one. In order to test if linalool plays a role in the behavioural responses, we assayed this compound in combination with the tropical hybrid, to provide other contextual olfactory cues. D. maidis was attracted to the tropical hybrid plus a 0.0001% linalool solution, indicating that this compound could be part of a blend of attractants. Whereas addition of linalool resulted in a slight, though not significant, reduction in host VOC attractiveness for P. maidis. Both hopper species responded to olfactory cues in the absence of supplementary visual cues.

Keywords

Auchenorrhynchavolatile organic compoundsolfactometryleafhopperplanthopper
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 109 , Issue 5 , October 2019 , pp. 633 - 642
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Copyright
Copyright © Cambridge University Press 2019 

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References

Adams, R.P. (2007) Identification of Essential Oil Components by Gas Chromatography/Quadrupole Mass Spectrometry. 4th edn. Carol Stream, Illinois, USA, Allured Publishing Corporation.Google Scholar
Argüello Caro, E.B., Maroniche, G.A., Analía, D., Sagadín, M.B., Del Vas, M. & Truol, G. (2013) High viral load in the planthopper vector Delphacodes kuscheli (Hemiptera: Delphacidae) is associated with successful transmission of Mal de Río Cuarto virus. Annals of the Entomological Society of America 106, 93–99.Google Scholar
Arneodo, J.D., Guzmán, F.A., Conci, L.R., Laguna, I.G. & Truol, G.A. (2002) Transmission features of Mal de Río Cuarto virus in wheat by its planthopper vector Delphacodes kuscheli. Annals of Applied Biology 141, 195–200.Google Scholar
Bento, J.M.S. (2008) Attraction of Bucephalogonia xanthophis (Hemiptera: Cicadellidae) to volatiles of its natural host Vernonia condensata (Asteraceae). Scientia Agricola (Piracicaba, Braz.) 65, 634–638.Google Scholar
Bullas-Appleton, E.S., Otis, G., Gillard, C. & Schaafsma, A.W. (2004) Potato leafhopper (Homoptera: Cicadellidae) varietal preferences in edible beans in relation to visual and olfactory cues. Environmental Entomology 33, 1381–1388.Google Scholar
Carloni, E., Carpane, P., Paradell, S., Laguna, I. & Gimenez Pecci, M.P. (2013) Presence of Dalbulus maidis (Hemiptera: Cicadellidae) and of Spiroplasma kunkelii in the temperate region of Argentina. Journal of Economic Entomology 106, 1574–1581.Google Scholar
Carpane, P. & Ingrassia, H. (2012) Análisis del daño por Achaparramiento en híbridos de maíz. TCM. Internal communication MONSANTO ARGENTINA S.A.I.C.Google Scholar
Cook, A.G. & Denno, R.F. (1994) Planthopper–plant interactions: feeding behavior, plant nutrition, plant defense, and host plant specialization. pp. 114–139 in Denno, R.F. & Perfect, T.J. (Eds) Planthoppers: Their Ecology and Management. , Boston, Springer.Google Scholar
Cook, S.M., Khan, Z.R. & Pickett, J.A. (2007) The use of push-pull strategies in integrated pest management. Annual Review of Entomology 52, 375–400.Google Scholar
Compton, S.G. (2002) Sailing with the wind: dispersal by small flying insects. pp. 113–133 in Bullock, J.M., Kenward, R.E. & Hails, R.S. (Eds) Dispersal Ecology. Cambridge, Cambridge University Press.Google Scholar
Davila-Flores, A.M., DeWitt, T.J. & Bernal, J.S. (2013) Facilitated by nature and agriculture: performance of a specialist herbivore improves with host-plant life history evolution, domestication, and breeding. Oecologia 173, 1425–1437.Google Scholar
Diaz, C.N., Luft Albarracín, E. & Alderete, M. (2016) Preferencia de oviposición de Peregrinus maidis (Hemiptera: Delphacidae) en distintas plantas hospederas. Revista de la Sociedad Entomologica Argentina 75, 139–146.Google Scholar
Fereres, A. & Moreno, A. (2009) Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Research 141, 158–168.Google Scholar
Gimenez Pecci, M.P., Laguna, I.G. & Lenardón, S. (2012) Enfermedades del maíz producidas por Virus y Mollicutes en Argentina. Ediciones INTA Buenos Aires, Argentina. ISBN 978-987-679-116-8.Google Scholar
Hassanali, A., Herren, H., Khan, Z.R., Pickett, J.A. & Woodcck, C.M. (2008) Integrated pest management: the push–pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 363, 611–621.Google Scholar
He, P., Zhang, J., Liu, N.Y., Zhang, Y.N., Yang, K. & Dong, S.L. (2011) Distinct expression profiles and different functions of odorant binding proteins in Nilaparvata lugens Stal. PLoS ONE 6(12), e28921. https://doi.org/10.1371/journal.pone.0028921.Google Scholar
He, M., Zhang, Y.N. & He, P. (2015) Molecular characterization and differential expression of an olfactory receptor gene family in the white-backed Planthopper Sogatella furcifera based on transcriptome analysis. PLoS ONE 10(11), e0140605. https://doi.org/10.1371/journal.pone.0140605.Google Scholar
Khan, Z.R. & Saxena, R.C. (1985) Effect of steam distillate extracts of a resistant rice variety on feeding behaviour of Nephotettix virescens (Homoptera: Cicadellidae). Journal of Economic Entomology 78, 562–566.Google Scholar
Krokos, F.D., Konstantopoulou, M.A. & Mazomenos, B.E. (2002) Chemical characterisation of corn plant compounds by different extraction techniques and the role of potent chemicals in the reproductive behaviour of the corn stalk borer Sesamia nonagrioides. Use of pheromones and other semiochemicals in integrated production. IOBC-WPRS Bulletin 25, 1–9.Google Scholar
La Grange, M.R. (2016) Olfactory responses of the leafhopper vector, Mgenia fuscovaria Stål (Hemiptera: Cicadellidae), to volatiles from aster yellows phytoplasma-infected and uninfected grapevine (Vitis vinifera L.). Dissertation, University of Pretoria.Google Scholar
La Grange, R., Schröder, M., Glinwood, R., Ignell, R. & Krüger, K. (2017) Leafhopper interactions with host plants – a role for volatile cues? IOBC-WPRS Bulletin 126, 22–26.Google Scholar
Lenardon, S.L., March, G.J., Nome, S.F. & Ornaghi, J.A. (1998) Recent outbreak of ‘Mal de Rio Cuarto’ virus on corn in Argentina. Plant Disease 82, 448–448.Google Scholar
Liu, G., Saxena, R.C. & Wilkins, R.M. (1994) Behavioral responses of the Whitebacked Planthopper Sogatella furcifera (Homoptera: Delphacidae) on rice plants whose odors have been masked. Journal of Insect Behavior 7, 343–353.Google Scholar
Luft Albarracin, E., Paradell, S. & Virla, E. (2008) Cicadellidae (Hemiptera: Auchenorrhyncha) associated to maize crops in north-western Argentina, influence of the sowing date and phenology on the abundance and diversity. Maydica 53, 289–296.Google Scholar
Luft Albarracin, E., Triapitsyn, S.V. & Virla, E.G. (2017) Egg parasitoids of the corn leafhopper, Dalbulus maidis (Delong) (Hemiptera: Cicadellidae), in Argentina. Neotropical Entomology 46, 666–677.Google Scholar
Marino de Remes Lenicov, A.M. & Paradell, S.L. (2012) Morfología y biología de especies vectoras de virus y mollicutes al maíz en la Argentina (Insecta-Hemiptera-Cicadomorpha-Fulgoromorpha). pp. 125–152 in Giménez Pecci, M.P., Laguna, I.G. & Lenardón, S. (Eds), Enfermedades del maíz producidas por Virus y Mollicutes en Argentina. Argentina, Ediciones INTA Buenos Aires, ISBN 978-987-679-116-8.Google Scholar
Mazzoni, V., Ioriatti, C., Trona, F., Lucchi, A., De Cristofaro, A. & Anfora, G. (2009) Study on the role of olfaction in host plant detection of Scaphoideus titanus (Hemiptera: Cicadellidae) Nymphs. Journal of Economic Entomology 102, 974–980.Google Scholar
McKamey, S. (2002) Leafhoppers of the world database: progress report. p. 85 in Hoch, H., Asche, M., Homberg, C. & Kessling, P. (Eds) Proceedings of the 11th International Auchenorrhyncha Congress, 5–9 August 2002, Postdam, Berlin, Germany.Google Scholar
Molnár, B.P., Tóth, Z., Fejes-Tóth, A., Dekker, T. & Kárpáti, Z. (2015) Electrophysiologically-active maize volatiles attract gravid female European Corn Borer, Ostrinia nubilalis. Journal of Chemical Ecology 41, 997–1005.Google Scholar
Nault, L.R. (1983) Origin of leafhopper vectors of maize pathogens in Mesoamerica. pp. 75–78 in Proceedings of the International Maize Virus Diseases Colloquium and Workshop. Wooster, Ohio, USA, Ohio Agricultural Research and Development Center.Google Scholar
Nault, L.R. & Rodríguez, J. (1985) The Leafhoppers and Planthoppers. New York, John Wiley & Sons Inc., p. 485.Google Scholar
Obata, T., Koh, H.S., Kim, M. & Fukami, H. (1981) Planthopper attractants in rice plant. Applied Entomology and Zoology 25, 47–51.Google Scholar
Obata, T., Koh, H.S., Kim, M. & Fukami, H. (1983) Constituents of planthopper attractant in rice plant. Applied Entomology and Zoology 18, 161–169.Google Scholar
Oliveira, C.M., Lopes, J.R.S. & Nault, L.R. (2013) Survival strategies of Dalbulus maidis during maize off-season in Brazil. Entomologia Experimentalis et Applicata 147, 141–153.Google Scholar
Oluwafemi, S., Bruce, T.J.A., Pickett, J.A., Ton, J. & Birkett, M.A. (2011) Behavioral responses of the leafhopper, Cicadulina storeyi China, a major vector of maize streak virus, to volatile cues from intact and leafhopper-damaged maize. Journal of Chemical Ecology 37, 40–48.Google Scholar
Oluwafemi, S., Birkett, M.A., Caulfield, J. & Pickett, J.A. (2012) Variability of volatile organic compounds emitted by seedlings of seven African maize varieties when infested by adult Cicadulina storeyi China leafhopper vectors of maize streak virus. African Crop Science Journal 20, 117–124.Google Scholar
Paradell, S.L., Virla, E.G. & Toledo, A. (2001) Leafhoppers species richness and abundance on corn crops in Argentina (Insecta-Hemiptera-Cicadellidae). Boletin Sanidad Vegetal Plagas 27, 465–474.Google Scholar
Patt, J.M. & Setamou, M. (2007) Olfactory and visual stimuli affecting host plant detection in Homalodisca coagulata (Hemiptera: Cicadellidae). Environmental Entomology 36, 142–150.Google Scholar
Potter, T.L., Olson, D.M., Ni, X. & Rains, G.C. (2015) A re-examination of corn (Zea mays L.) ear volatiles. Phytochemistry Letters 14, 280–286.Google Scholar
Ranger, C.M., Winter, R.E.K., Backus, E.A., Rottinghaus, G.E., Ellersieck, M.R. & Johnson, D.W. (2005) Discrimination by potato leafhopper (Hemiptera: Cicadellidae) of host volatiles from resistant and susceptible alfalfa, Medicago sativa L. Environmental Entomology 34, 271–280.Google Scholar
Robert, C.A.M., Erb, M., Hiltpold, I., Hibbard, B.E., Gaillard, M.D.P., Bilat, J., Degenhardt, J., Cambet-Petit-Jean, X., Turlings, T.C.J. & Zwahlen, C. (2013) Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field. Plant Biotechnology Journal 1, 1–12.Google Scholar
Saxena, K.N. & Saxena, R.C. (1974) Patterns of relationships between certain leafhoppers and plants, part II. Role of sensory stimuli in orientation and feeding. Entomologia Experimentalis et Applicata 17, 493–503.Google Scholar
Singh, B.U. & Seetharama, N. (2008) Host plant interactions of the corn planthopper, Peregrinus maidis Ashm. (Homoptera: Delphacidae) in maize and sorghum agroecosystems. Arthropod Plant Interactions 2, 163–196.Google Scholar
Theodorou, V., Skobridis, K., Tzakos, A.G. & Ragoussis, V. (2007) A simple method for the alkaline hydrolysis of esters. Tetrahedron Letters 48, 8230–8233.Google Scholar
Tsai, J.H. (1996) The development and oviposition of Peregrinus maidis (Ashmead) (Homoptera: Delphacidae) on various host plants. Florida Entomologist 79, 19–26.Google Scholar
Todd, J.L., Phelan, P.L. & Nault, L.R. (1990) Interaction between visual and olfactory stimuli during host-finding by leafhopper, Dalbulus maidis (Homoptera: Cicadellidae). Journal of Chemical Ecology 16, 2121–2133.Google Scholar
Virla, E., Díaz, C., Carpane, P., Laguna, I., Ramallo, J., Gómez, L. & Giménez Pecci, M.P. (2004 a) Evaluación preliminar de la disminución en la producción de maíz causada por el ‘Corn Stunt Spiroplasma’ (CSS) en Tucumán, Argentina. Boletin Sanidad Vegetal Plagas 30, 403–413.Google Scholar
Virla, E., Miotti, I., Giménez Pecci, M.P., Carpane, P. & Laguna, G. (2004 b). Peregrinus maidis (Hemiptera: Delphacidae), new experimental vector of the ‘Mal de Río Cuarto’ disease to corn. Biocell 28, 54.Google Scholar
Virla, E.M., Casuso, M. & Frias, E. (2010) A preliminary study on the effects of a transgenic corn event on the non-target pest Dalbulus maidis (Hemiptera: Cicadellidae). Crop Protection 29, 635–638.Google Scholar
Virla, E.G., Moya Raygoza, G. & Luft Albarracin, E. (2013) Egg parasitoids of the corn leafhopper, Dalbulus maidis, in the southernmost area of its distribution range. Journal of Insect Science 13, 1–7.Google Scholar
Wang, B., Zhou, G., Xin, Z., Ji, R. & Lou, Y. (2015) (Z)-3-Hexenal, one of the green leaf volatiles, increases susceptibility of rice to the white-backed Planthopper Sogatella furcifera. Plant Molecular Biology Reporter 33, 377–387.Google Scholar
Youn, Y. (2002) Electroantennogram responses of Nilaparvata lugens (Homoptera: Delphacidae) to plant volatile compounds. Journal of Economic Entomology 95, 269–277.Google Scholar
Zhang, X., Pengsakul, T., Tukayo, M., Yu, L., Fang, W. & Luo, D. (2017) Host-location behavior of the tea green leafhopper Empoasca vitis Göthe (Hemiptera: Cicadellidae): olfactory and visual effects on their orientation. Bulletin of Entomological Research 25, 1–11.Google Scholar
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