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Sulfur volatiles from Allium spp. affect Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), response to citrus volatiles

Published online by Cambridge University Press:  08 July 2010

R.S. Mann ,
R.L. Rouseff ,
J.M. Smoot ,
W.S. Castle  and
L.L. Stelinski
R.S. Mann
Affiliation:
Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred, FL33850, USA
R.L. Rouseff
Affiliation:
Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred, FL33850, USA
J.M. Smoot
Affiliation:
Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred, FL33850, USA
W.S. Castle
Affiliation:
Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred, FL33850, USA
L.L. Stelinski*
Affiliation:
Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred, FL33850, USA
*
*Author for correspondence Fax: 863-956-4631 E-mail: [email protected]
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Abstract

The Asian citrus psyllid, Diaphorina citri Kuwayama, vectors Candidatus Liberibacter asiaticus (Las) and Candidatus Liberibacter americanus (Lam), the presumed causal agents of huanglongbing. D. citri generally rely on olfaction and vision for detection of host cues. Plant volatiles from Allium spp. (Alliaceae) are known to repel several arthropod species. We examined the effect of garlic chive (A. tuberosum Rottl.) and wild onion (A. canadense L.) volatiles on D. citri behaviour in a two-port divided T-olfactometer. Citrus leaf volatiles attracted significantly more D. citri adults than clean air. Volatiles from crushed garlic chive leaves, garlic chive essential oil, garlic chive plants, wild onion plants and crushed wild onion leaves all repelled D. citri adults when compared with clean air, with the first two being significantly more repellent than the others. However, when tested with citrus volatiles, only crushed garlic chive leaves and garlic chive essential oil were repellent, and crushed wild onions leaves were not.

Analysis of the headspace components of crushed garlic chive leaves and garlic chive essential oil by gas chromatography-mass spectrometry revealed that monosulfides, disulfides and trisulfides were the primary sulfur volatiles present. In general, trisulfides (dimethyl trisulfide) inhibited the response of D. citri to citrus volatiles more than disulfides (dimethyl disulfide, allyl methyl disulfide, allyl disulfide). Monosulfides did not affect the behaviour of D. citri adults. A blend of dimethyl trisulfide and dimethyl disulfide in 1:1 ratio showed an additive effect on inhibition of D. citri response to citrus volatiles. The plant volatiles from Allium spp. did not affect the behaviour of the D. citri ecto-parasitoid Tamarixia radiata (Waterston). Thus, Allium spp. or the tri- and di-sulphides could be integrated into management programmes for D. citri without affecting natural enemies.

Keywords

Diaphorina citriTamarixia radiatagarlic chivedimethyl trisulfidedimethyl disulfidecitrus
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 101 , Issue 1 , February 2011 , pp. 89 - 97
Copyright
Copyright © Cambridge University Press 2010

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References

Amarawardana, L., Bandara, P., Kumar, V., Pettersson, J., Ninkovic, V. & Glinwood, R. (2007) Olfactory response of Myzus persicae (Homoptera: Aphididae) to volatiles from leek and chive: potential for intercropping with sweet pepper. Acta Agriculturae Scandinavia B 57, 87–91.Google Scholar
Arimura, G., Ozawa, R., Shimoda, T., Nishioka, T., Boland, W. & Takabayashi, J. (2000) Herbivory-induced volatiles elicit defense genes in lima bean leaves. Nature 406, 512–515.CrossRefGoogle ScholarPubMed
Arthur, F.H. (1996) Grain protectants: current status and prospects for the future. Journal of Stored Product Research 32, 293–302.CrossRefGoogle Scholar
Assis, F.A., Moraes, J.C. & Assis, G.A. (2007) Effect of the aqueous extract of garlic bulbs on the aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae) on potato. Ecossistema 3, 63–66.Google Scholar
Aubert, B. (1990) Integrated activities for the control of huanglongbinggreening and its vector Diaphorina citri Kuwayama in Asia. pp. 133–144 in Aubert, B., Tontyaporn, S. & Buangsuwon, D. (Eds) Proceedings of the Fourth FAO-UNDP International Asia Pacific Conference on Citrus Rehabilitation, 4–10 February 1990, Chiang Mai, Thailand.Google Scholar
Auger, J., Lecomte, C. & Thibout, E. (1989) Leek odour analysis by gas chromatography and identification of most active substance for leek moth Acrolipeopsis assectella. Journal of Chemical Ecology 15, 1847–1854.CrossRefGoogle ScholarPubMed
Beattie, G.A.C., Holford, P., Mabberley, D.J., Haigh, A.M., Bayer, R. & Broadbent, P. (2006) Aspects and insights of Australia-Asia collaborative research on huanglongbing. pp. 47–64 in Proceedings of the International Workshop for the Prevention of Citrus Greening Disease in Severely Infected Areas, 7–9 December 2006, International Research Division, Ishigaki, Japan.Google Scholar
Block, E. (2005) Biological activity of Allium compounds: recent results. Acta Horticulture 688, 41–57.CrossRefGoogle Scholar
Bové, J.M. (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology 88, 7–37.Google Scholar
Capoor, S.P. (1963) Decline of citrus trees in India. Bulletin of National Institute of Science India 24, 48–64.Google Scholar
Catling, H.D. (1970) Distribution of psyllid vectors of citrus greening disease with notes on the biology and bionomics of Diaphorina citri. FAO Plant Protection Bulletin 18, 8–15.Google Scholar
Childers, C.C. & Rogers, M.E. (2005) Chemical control and management approaches of the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae) in Florida citrus. Proceedings of Florida State Horticultural Society 118, 49–53.Google Scholar
Dicke, M. & van Loon, J.J.A. (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomologia Experimentalis et Applicata 97, 237–244.CrossRefGoogle Scholar
Dugravot, S., Sanon, A., Thibout, E. & Huignard, J. (2002) Susceptibility of Callosobruchus maculatus (Coleoptera: Bruchidae) and its parasitoid Dinarmus basalis (Hymenoptera: Pteromalidae) to sulfur-containing compounds: consequences on biological control. Environmental Entomology 31, 550–557.CrossRefGoogle Scholar
Dugravot, S., Grolleau, F., Macherel, D., Rochetaing, A., Hue, B., Stankiewicz, M., Huignard, J. & Lapied, B. (2003) Dimethyl disulfide exerts insecticidal neurotoxicity through mitochondrial dysfunction and activation of insect KATP channels. Journal of Neurophysiology 90, 259–270.CrossRefGoogle Scholar
Dugravot, S., Thibout, E., Abo-ghalia, A. & Huignard, J. (2004) How a specialist and a nonspecialist insect cope with the dimethyl disulfide produced by Allium porrum. Entomologia Experimentalis et Applicata 113, 173–179.CrossRefGoogle Scholar
Dugravot, S., Mondy, N., Mandon, N. & Thibout, E. (2005) Increased sulfur precursors and volatiles production by the leek Allium porrum in response to specialist insect attack. Journal of Chemical Ecology 31, 1573–1561.CrossRefGoogle ScholarPubMed
Gurusubramanian, G. & Krishna, S.S. (1996) The effects of exposing eggs of four cotton insect pests to volatiles of Allium sativum (Liliaceae). Bulletin of Entomological Research 86, 29–31.CrossRefGoogle Scholar
Halbert, S.E. & Manjunath, K.L. (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Florida Entomologist 87, 330–353.CrossRefGoogle Scholar
Hall, D.G. & Albrigo, L.G. (2007) Estimating the relative abundance of flush shoots in citrus, with implications on monitoring insects associated with flush. Horticulture Science 42, 364–368.Google Scholar
Hall, D.G., Gottwald, T.R., Nguyen, N.C., Ichinose, K., Le, Q.D., Beattie, G.A.C. & Stover, E. (2008) Greenhouse investigations on the effect of guava on infestations of Asian citrus psyllid in grapefruit. Proceedings of Florida State Horticultural Society 121, 104–109.Google Scholar
Hodges, A.C. & Morse, J.C. (2009) Southern plant diagnostic network invasive arthropod workshop, May 7–9, 2007. Journal of Insect Science 9, 61.CrossRefGoogle Scholar
Hoy, M.A. & Nguyen, R. (2001) Classical biological control of Asian citrus psylla. Citrus Industry 81, 48–50.Google Scholar
Hrutfiord, B.F., Hopley, S.M. & Gara, R.I. (1974) Monoterpenes in sitka spruce: within tree and seasonal variation. Phytochemistry 13, 2167–2170.CrossRefGoogle Scholar
Huang, Y., Chen, S.X. & Ho, S.H. (2000) Bioactivities of methyl allyl disulfide and diallyl trisulfide from essential oil of garlic to two species of stored-product pests, Sitophilus zeamais (Coleoptera: Curculionidae) and Tribolium castaneum (Coleoptera: Tenebrionidae). Journal of Economic Entomology 93, 537–543.CrossRefGoogle ScholarPubMed
Kristoffersen, L., Hallberg, E., Walle′n, R. & Anderbrant, O. (2006) Sparse sensilla array on Trioza apicalis (Homoptera: Triozidae) antennae: an adaptation to high stimulus level? Arthropod Structure and Development 35, 85–92.CrossRefGoogle Scholar
Landolt, P.J., Hofstetter, R.W. & Biddick, L.L. (1999) Plant essential oils as arrestants and repellents for neonate larvae of the codling moth (Lepidoptera: Tortricidae). Environmental Entomology 28, 954–960.CrossRefGoogle Scholar
Moran, V.C. & Brown, R.P. (1973) The antennae, host plant chemoreception and probing activity of the citrus psylla, Trioza erytreae (Del Guercio) (Homoptera: Psyllidae). Journal of Entomological Society of South Africa 36, 191–202.Google Scholar
Norris, D.M., Rozental, J.M., Samberg, G. & Singer, G. (1977) Protein-sulfur dependent differences in the nerve receptors for repellent 1,4-naphthoquinones in two strains of Periplaneta americana. Comparative Biochemistry and Physiology 57, 55–59.Google Scholar
Onagbola, E.A., Boina, D.R., Herman, S.L. & Stelinski, L.L. (2009) Antennal sensilla of Tamarixia radiata (Hymenoptera: Eulophidae), a parasitoid of Diaphorina citri (Hemiptera: Psyllidae). Annals of Entomological Society of America 102, 523–531.CrossRefGoogle Scholar
Podskalska, H., Ruzicka, J., Hoskovec, M. & Salek, M. (2009) Use of infochemicals to attract carrion beetles into pitfall traps. Entomologia Experimentalis et Applicata 132, 59–64.CrossRefGoogle Scholar
Powell, C.A., Burton, M.S., Pelpsi, M.A. & Bullock, R.C. (2007) Effects of insecticide on Asian citrus psyllid (Hemiptera: Psyllidae) populations in a Florida citrus grove. Plant Health Progress. http://www.plantmanagementnetwork.org/php/ (accessed 24 May 2010).CrossRefGoogle Scholar
Prowse, G.M., Galloway, T.S. & Foggo, A. (2006) Insecticidal activity of garlic juice in two dipteran pests. Agricultural and Forest Entomology 8, 1–6.CrossRefGoogle Scholar
Qureshi, J.A. & Stansly, P.A. (2007) Integrated approaches for managing the Asian citrus psyllid Diaphorina citri (Homoptera: Psylidae) in Florida. Proceedings of Florida State Horticultural Society 120, 110–115.Google Scholar
Qureshi, J.A., Rogers, M.E., Hall, D.G. & Stansly, P.A. (2009) Incidence of invasive Diaphorina citri (Hemiptera: Psyllidae) and its introduced parasitoid Tamarixia radiata (Hymenoptera: Eulophidae) in Florida citrus. Journal of Economic Entomology 102, 247–256.CrossRefGoogle Scholar
Rogers, M.E. (2008) General pest management considerations – responses to greening and its vectors have modified pest management programmes. Citrus Industry 89, 12–17.Google Scholar
Rogers, M.E. & Timmer, L.W. (2007) Florida pest management guide update. Citrus Industry 88, 11–12.Google Scholar
Rouseff, R.L., Onagbola, E.O., Smoot, J.M. & Stelinski, L.L. (2008) Sulfur volatiles in guava (Psidium guajava L.) leaves: possible defense mechanism. Journal of Agricultural and Food Chemistry 56, 8905–8910.CrossRefGoogle ScholarPubMed
Salas, J. (2001) Efficacy of a garlic based repellent on the reduction of whitefly (Bemisia tabaci) populations. Agronomia Tropical (Maracay) 51, 163–174.Google Scholar
Snow, K. & Cutler, R. (2006) A preliminary note on the evaluation of garlic as a mosquito repellent. European Mosquito Bulletin 21, 23–24.Google Scholar
Valerio, L. & Maroli, M. (2005) Evaluation of repellent and anti-feeding effect of garlic oil (Allium sativum) against the bite of phlebotomine sandflies Diptera: Psychodidae. Annali dell'Istituto Superiore di Sanita 41, 243–256.Google ScholarPubMed
Wenninger, E.J. & Hall, D.G. (2007) Daily timing of mating and age at reproductive maturity in Diaphorina citri (Hemiptera: Psyllidae). Florida Entomologist 90, 715–722.CrossRefGoogle Scholar
Wenninger, E.J., Stelinski, L.L. & Hall, D.G. (2009) Roles of olfactory cues, visual cues, and mating status in orientation of Diaphorina citri kuwayama (Hemiptera: Psyllidae) to four different host plants. Environmental Entomology 38, 225–234.CrossRefGoogle ScholarPubMed
Zaka, S.M., Zeng, X.N., Holford, P. & Beattie, G.A.C. (2010) Repellent effect of guava leaf volatiles on settlement of adults of citrus psylla, Diaphorina citri Kuwayama, on citrus. Insect Science 17, 39–45.CrossRefGoogle Scholar