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Arthropod-Plant Interactions

, Volume 11, Issue 5, pp 709–716 | Cite as

Curry leaf smells better than citrus to females of Diaphorina citri (Hemiptera: Liviidae)

  • V. H. BelotiEmail author
  • F. Santos
  • G. R. Alves
  • J. M. S. Bento
  • P. T. Yamamoto
Original Paper

Abstract

The Asian citrus psyllid (ACP) Diaphorina citri Kuwayama has a host range of about 20 species of the family Rutaceae, including Citrus spp. However, few studies have reported on its host preference. This study evaluated the host-choice behavior of ACP in curry leaf (Murraya koenigii L.), through free-choice test and bioassays with a type ‘Y’ olfactometer, and also characterized the volatiles involved in attracting the ACP. In the free-choice test, the number of adults per plant on curry leaf was higher than the number on citrus plants. When the ACP was tested in the olfactometer, the females showed preference for curry leaf over citrus plants. Sixteen volatile compounds were identified in citrus and curry leaves. Qualitative and quantitative differences in the compounds released by citrus and curry leaves were determined. The volatiles present in these hosts may play an important role in the attraction of D. citri. With this information, further studies should be done to develop new management strategies for the ACP.

Keywords

Huanglongbing Volatiles Terpenes Asian citrus psyllid Rutaceae 

Notes

Acknowledgements

This study was supported by the National Institute of Science and Technology (INCT) Semiochemicals in Agriculture (Fapesp Proc. 2008/57701-2 and CNPq Proc. 573761/2008-6). VHB is supported by FAPESP (Process 2013/25157-0). The authors also thank K.F. Martins and M.M. Picoli for assistance during the bioassays, A.P. Favaris for technical assistance with the GC analysis, and D.L.P. Schorkopf for comments in final version.

Supplementary material

11829_2017_9524_MOESM1_ESM.docx (44 kb)
Supplementary material 1 (DOCX 45 kb)

References

  1. Alves GR, Diniz AJF, Parra JRP (2014) Biology of the huanglongbing vector Diaphorina citri (Hemiptera: Liviidae) on different host plants. J Econ Entomol 107:691–696CrossRefPubMedGoogle Scholar
  2. Arrebola ML (1997) Principal components analysis of essential oils. In: Linskens HF, Jackson JF (eds) Modern methods of plant analysis. Springer, Berlin, pp 159–174Google Scholar
  3. Aubert B (1987) Trioza erytreae Del Guercio and Diaphorina citri Kuwayama (Homoptera: Psyllidae), the two vectors of citrus greening disease: biological aspects and possible control strategies. Fruits 42:149–162Google Scholar
  4. Baldwin IT (2010) Plant volatiles. Curr Biol 20:392–397CrossRefGoogle Scholar
  5. Ballhorn DJ, Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect defenses of lima bean (Phaseolus lunatus). J Ecol 96:971–980CrossRefGoogle Scholar
  6. Belasque J Jr, Bassanezi RB, Yamamoto PT, Ayres AJ, Tachibana A, Violonte AR, Tank A Jr, Giorgis F, Tersi FEA, Menezes GM, Dragone J, Jank RH Jr, Bové JM (2010) Lessons from Huanglongbing management in São Paulo State, Brazil. J Plant Pathol 2:285–302Google Scholar
  7. Beloti VH, Alves GR, Araújo DFD, Picoli MM, Moral RA, Demétrio CGB, Yamamoto PT (2015) Lethal and sublethal effects of insecticides used on citrus, on the ectoparasitoid Tamarixia radiata. PLoS ONE 10(7):e0132128. doi: 10.1371/journal.pone.0132128 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bergström G, Rothschild M, Groth I, Crighton K (1995) Oviposition by butterflies on young leaves: investigation of leaf volatiles. Chemoecology 5:147–158Google Scholar
  9. Chakraborty NK, Pandey PK, Chatterjee SN, Singh AB (1976) Host preference in Diaphorina citri Kuwayama vector of greening disease of citrus in India. Indian J Entomol 38:196–197Google Scholar
  10. Chakravarthi VP, Savithri P, Rajendra Prasad P, Venugopal Rao N (1998) Biology and seasonal abundance of citrus psylla Diaphorina citri Kuwayama (Homoptera: Psyllidae). In: National Symposium of Pest Management of Horticultural Crops. Bangalore, pp 26–29Google Scholar
  11. Damsteegt VD, Postnikova EN, Stone AL, Kuhlmann M, Wilson C, Sechler A, Schaad NW, Brlansky RH, Scheneider WL (2010) Murraya paniculata and related species as potential hosts and inoculum reservoirs of “Candidatus Liberibacter asiaticus”, causal agent of Huanglongbing. Plant Dis 94:528–533CrossRefGoogle Scholar
  12. Diniz AJF (2013) Otimização da criação de Diaphorina citri Kuwayama, 1908 (Hemiptera: Liviidae) e de Tamarixia radiata (Waterston, 1922) (Hymenoptera: Eulophidae), visando a produção em larga escala do parasitoide e avaliação do seu estabelecimento em campo. PhD Thesis, “Luiz de Queiroz” College of Agriculture/University of São Paulo (ESALQ/USP)Google Scholar
  13. Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gancel AL, Ollitrault P, Froelicher Y, Tomi F, Jacquemond C, Brillouet JM (2003) Leaf volatile compounds of seven citrus somatic tetraploid hybrids sharing willow leaf mandarin (Citrus deliciosa Ten.) as their common parent. J Agric Food Chem 51:6006–6013CrossRefPubMedGoogle Scholar
  15. Gottwald TR (2010) Current epidemiological understanding of citrus huanglongbing. Annu Rev Phytopathol 48:119–139CrossRefPubMedGoogle Scholar
  16. Grafton-Cardwell E, Stelinski LL, Stansly PA (2013) Biology and management of asian citrus psyllid, vector of the Huanglongbing pathogens. Ann Rev Entomol 58:413–432CrossRefGoogle Scholar
  17. Halbert SE, Manjunath KL (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Fla Entomol 3:330–353CrossRefGoogle Scholar
  18. Hall DG, Albrigo LG (2007) Estimating the relative abundance of flush shoots in citrus, with implications on monitoring insects associated with flush. Hort Sci 42:364–368Google Scholar
  19. Hodkinson ID (2009) Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): a global synthesis. J Nat Hist 1–2:65–179CrossRefGoogle Scholar
  20. Hori M (1999) Antifeeding, settling inhibitory and toxic activities of labiate essential oils against the green peach aphid, Myzus persicae (Sulzer) (Homoptera: Aphididae). Appl Entomol Zool 34:113–118CrossRefGoogle Scholar
  21. Jung JS (2014) Analysis of volatile compounds in the root peel, stem peel, and fruit peel of pomegranate (Punica granatum) by TD GC/MS. Int J BioSci BioTechnol 6:169–182Google Scholar
  22. Keeling CI, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the consti-tutive and induced defence of conifers against insects and pathogens. New Phytol 170:657–675CrossRefPubMedGoogle Scholar
  23. Lira ACS, Zanardi OZ, Beloti VH, Bordini GP, Yamamoto PT, Parra JRP, Carvalho GA (2015) Lethal and sublethal impacts of acaricides on Tamarixia radiata (Hemiptera: Eulophidae), an important ectoparasitoid of Diaphorina citri (Hemiptera: Liviidae). J Econ Entomol 108:2278–2288CrossRefPubMedGoogle Scholar
  24. Macleod AJ, Pieris NM (1982) Analysis of the volatile essential oils of Murraya koenigii and Pandanus latifolius. Phytochemistry 21:1653–1657CrossRefGoogle Scholar
  25. Metcalf RL, Metcalf ER (1992) Plant kairomones in insect ecology and control. Chapman and Hall, New YorkGoogle Scholar
  26. Moran VC (1968) The development of the citrus psylla, Trioza erytreae (Del Guercio) (Homoptera: Psyllidae), on Citrus limon and four indigenous host plants. J Entomol Soc South Africa 31:390–402Google Scholar
  27. Moran VC, Buchan PR (1975) Oviposition by the citrus psylla, Trioza erytreae (Homoptera: Psyllidae), in relation to leaf hardness. Entomol Exp Appl 18:96–104CrossRefGoogle Scholar
  28. Nava DE, Torres MLG, Rodrigues MDL, Bento JMS, Parra JRP (2007) Biology of Diaphorina citri (Hem., Psyllidae) on different hosts and different temperatures. J Appl Entomol 131:709–715CrossRefGoogle Scholar
  29. Ngoh SP, Choo LEW, Pang FY, Huang Y, Kini MR, Ho SH (1998) Insecticidal and repellent properties of nine volatile constituents of essential oils against the American cockroach, Periplaneta americana (L.). Pestic Sci 54:261–268CrossRefGoogle Scholar
  30. Padmakumari KP (2009) Volatile constituents from the leaves and flowers of Murraya koenigii (Linn.) spreng. J Essent Oil Bear Pl 12:722–727CrossRefGoogle Scholar
  31. Paré PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331CrossRefPubMedPubMedCentralGoogle Scholar
  32. Parra JRP, Alves GR, Diniz AJF, Vieira JM (2016) Tamarixia radiata (Hymenoptera: Eulophidae) × Diaphorina citri (Hemiptera: Liviidae): mass rearing and potential use of the parasitoid in Brazil. JIPM 7:1–11CrossRefGoogle Scholar
  33. Patt JM, Sétamou M (2007) Olfactory and visual stimuli affecting host plant detection in Homalodisca coagulata (Hemiptera: Cicadellidae). Environ Entomol 36:142–150CrossRefPubMedGoogle Scholar
  34. Patt JM, Sétamou M (2010) Responses of the Asian citrus psyllid to volatiles emitted by flushing shoots of its rutaceous host plants. Environ Entomol 39:618–624CrossRefPubMedGoogle Scholar
  35. Prates HT, Santos JP, Waquil JM, Fabris JD, Oliveira AB, Foster JE (1998) Insecticidal activity of monoterpenes against Ryzopertha dominica (F.) and Tribolium castaneum (Herbst). J Stored Prod Res 34:243–249CrossRefGoogle Scholar
  36. Rajeswara Rao BB, Rajput DK, Mallavarapu GR (2011) Chemical diversity in curry leaf (Murraya koenigii) essential oils. Food Chem 126:989–994CrossRefGoogle Scholar
  37. Rice PJ, Coats JR (1994) Insecticidal properties of monoterpenoid derivatives to the house fly (Diptera: Muscidae) and red flour beetle (Coleoptera: Tenebrionidae). Pestic Sci 41:195–202CrossRefGoogle Scholar
  38. Robbins PS, Alessandro RT, Stelinski LL, Lapointe SL (2012) Volatile profiles of young leaves of Rutaceae spp. varying in susceptibility to the Asian citrus psyllid (Hemiptera: Psyllidae). Fla Entomol 95:774–776CrossRefGoogle Scholar
  39. Sétamou M, Flores D, French JV, Hall DG (2008) Dispersion patterns and sampling plans for Diaphorina citri (Hemiptera: Psyllidae) in citrus. J Econ Entomol 101:1478–1487CrossRefPubMedGoogle Scholar
  40. Sfara V, Zerba EN, Alzogaray RA (2009) Fumigant insecticidal activity and repellent effect of five essential oils and seven monoterpenes on first-instar nymphs of Rhodnius prolixus. J Med Entomol 46:511–515CrossRefPubMedGoogle Scholar
  41. Steinhaus M (2015) Characterization of the major odor-active compounds in the leaves of the curry tree Bergera koenigii L. by aroma extract dilution analysis. J Agric Food Chem 63:4060–4067CrossRefPubMedGoogle Scholar
  42. Stewart-Jones A, Poppy GM (2006) Comparison of glass vessels and plastic bags for enclosing living plant parts for headspace analysis. J Chem Ecol 32:845–864CrossRefPubMedGoogle Scholar
  43. R Development Core Team (2014) R: A language and environment for statistical computing. Vienna. Available: http://www.R-project.org/
  44. Teck SLC, Fatimah A, Beattie A, Heng RKJ, King WS (2011) Influence of host plant species and flush growth stage on the asian citrus psyllid, Diaphorina citri Kuwayama. AJABS 6:536–543Google Scholar
  45. Teixeira DC, Danet JL, Eveillard S, Martins EC, De Jesus Jr WC, Yamamoto PT, Lopes SA, Bassanezi RB, Ayres AJ, Saillard C, Bové JM (2005) Citrus huanglongbing in São Paulo, Brazil: PCR detection of the ‘Candidatus’ Liberibacter species associated with the disease. Mol Cell Probes 19:173–179CrossRefGoogle Scholar
  46. Tiwari S, Sayed RS, Sayed ME, Stelinski LL (2011) Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Manag Sci 67:1258–1268CrossRefPubMedGoogle Scholar
  47. Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671CrossRefPubMedGoogle Scholar
  48. Tsagkarakis EA, Rogers ME (2010) Suitability of ‘Cleopatra’ mandarin as a host plant for Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 93:451–453CrossRefGoogle Scholar
  49. Ukeh DA, Emosairie SO, Udo IA, Ofem UA (2007) Field evaluation of neem (Azadirachta indica A. Juss) products for the management of lepidopterous stem borers of maize (Zea mays L.) in Calabar. Res J Appl Sci 2:15–19Google Scholar
  50. van Dam NM, Qiu BL, Hordijk AC, Vet LEM, Jansen JJ (2010) Identification of biologically relevant compounds in aboveground and belowground induced volatile blends. J Chem Ecol 36:1006–1016CrossRefPubMedPubMedCentralGoogle Scholar
  51. Verma RS, Padalia RC, Arya V, Chauhan A (2012) Aroma profiles of the curry leaf, Murraya koenigii (L.) Spreng. chemotypes: variability in north India during the year. Ind Crop Prod 36:343–348CrossRefGoogle Scholar
  52. Wenninger EJ, Hall DG (2007) Daily timing of mating and age at reproductive maturity in Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 90:715–722CrossRefGoogle Scholar
  53. Wenninger EJ, Stelinski LL, Hall DG (2009) Role of olfactory cues, visual cues, and mating status in orientation of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) to four different host plants. Environ Entomol 38:225–234CrossRefPubMedGoogle Scholar
  54. Westbrook CJ, Hall DG, Stover E, Duan YP, Lee RF (2011) Colonization of citrus and citrus-related germplasm by Diaphorina citri (Hemiptera: Psyllidae). HortScience 46:997–1005Google Scholar
  55. Yamamoto PT, Bassanezi RB (2003) Seletividade de produtos fitossanitários aos inimigos naturais de pragas dos citros. Laranja 24:353–382Google Scholar
  56. Yamamoto PT, Alves GR, Beloti VH (2014) Manejo e controle do huanglongbing (HLB) dos cítricos. Investig Agrar 16:69–82Google Scholar
  57. Zaka SM, Zeng XN, Holford P, Beattie GAC (2010) Repellent effect of guava leaf volatiles on settlement of adults of citrus psylla, Diaphorina citri Kuwayama, on citrus. Insect Sci 17:35–45CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.Department of Entomology and Acarology‘Luiz de Queiroz’ College of Agriculture/University of São Paulo (ESALQ/USP)PiracicabaBrazil

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