Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alves GR, Diniz AJF, Parra JRP (2014) Biology of the huanglongbing vector Diaphorina citri (Hemiptera: Liviidae) on different host plants. J Econ Entomol 107:691–696

    Article  CAS  PubMed  Google Scholar 

  • Arrebola ML (1997) Principal components analysis of essential oils. In: Linskens HF, Jackson JF (eds) Modern methods of plant analysis. Springer, Berlin, pp 159–174

    Google Scholar 

  • 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 42:149–162

    Google Scholar 

  • Baldwin IT (2010) Plant volatiles. Curr Biol 20:392–397

    Article  Google Scholar 

  • Ballhorn DJ, Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect defenses of lima bean (Phaseolus lunatus). J Ecol 96:971–980

    Article  CAS  Google Scholar 

  • 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 2:285–302

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Bergström G, Rothschild M, Groth I, Crighton K (1995) Oviposition by butterflies on young leaves: investigation of leaf volatiles. Chemoecology 5:147–158

    Google Scholar 

  • 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 38:196–197

    Google Scholar 

  • 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 26–29

  • 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 94:528–533

    Article  CAS  Google Scholar 

  • 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)

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 51:6006–6013

    Article  CAS  PubMed  Google Scholar 

  • Gottwald TR (2010) Current epidemiological understanding of citrus huanglongbing. Annu Rev Phytopathol 48:119–139

    Article  CAS  PubMed  Google Scholar 

  • Grafton-Cardwell E, Stelinski LL, Stansly PA (2013) Biology and management of asian citrus psyllid, vector of the Huanglongbing pathogens. Ann Rev Entomol 58:413–432

    Article  CAS  Google Scholar 

  • 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 3:330–353

    Article  Google Scholar 

  • Hall DG, Albrigo LG (2007) Estimating the relative abundance of flush shoots in citrus, with implications on monitoring insects associated with flush. Hort Sci 42:364–368

    Google Scholar 

  • Hodkinson ID (2009) Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): a global synthesis. J Nat Hist 1–2:65–179

    Article  Google Scholar 

  • 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 34:113–118

    Article  CAS  Google Scholar 

  • 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 6:169–182

    Google Scholar 

  • 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 170:657–675

    Article  CAS  PubMed  Google Scholar 

  • 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 108:2278–2288

    Article  CAS  PubMed  Google Scholar 

  • Macleod AJ, Pieris NM (1982) Analysis of the volatile essential oils of Murraya koenigii and Pandanus latifolius. Phytochemistry 21:1653–1657

    Article  CAS  Google Scholar 

  • Metcalf RL, Metcalf ER (1992) Plant kairomones in insect ecology and control. Chapman and Hall, New York

    Google Scholar 

  • 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 31:390–402

    Google Scholar 

  • Moran VC, Buchan PR (1975) Oviposition by the citrus psylla, Trioza erytreae (Homoptera: Psyllidae), in relation to leaf hardness. Entomol Exp Appl 18:96–104

    Article  Google Scholar 

  • 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 131:709–715

    Article  Google Scholar 

  • 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 54:261–268

    Article  CAS  Google Scholar 

  • Padmakumari KP (2009) Volatile constituents from the leaves and flowers of Murraya koenigii (Linn.) spreng. J Essent Oil Bear Pl 12:722–727

    Article  CAS  Google Scholar 

  • Paré PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 7:1–11

    Article  Google Scholar 

  • Patt JM, Sétamou M (2007) Olfactory and visual stimuli affecting host plant detection in Homalodisca coagulata (Hemiptera: Cicadellidae). Environ Entomol 36:142–150

    Article  CAS  PubMed  Google Scholar 

  • Patt JM, Sétamou M (2010) Responses of the Asian citrus psyllid to volatiles emitted by flushing shoots of its rutaceous host plants. Environ Entomol 39:618–624

    Article  CAS  PubMed  Google Scholar 

  • 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 34:243–249

    Article  CAS  Google Scholar 

  • Rajeswara Rao BB, Rajput DK, Mallavarapu GR (2011) Chemical diversity in curry leaf (Murraya koenigii) essential oils. Food Chem 126:989–994

    Article  CAS  Google Scholar 

  • Rice PJ, Coats JR (1994) Insecticidal properties of monoterpenoid derivatives to the house fly (Diptera: Muscidae) and red flour beetle (Coleoptera: Tenebrionidae). Pestic Sci 41:195–202

    Article  CAS  Google Scholar 

  • 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 95:774–776

    Article  CAS  Google Scholar 

  • Sétamou M, Flores D, French JV, Hall DG (2008) Dispersion patterns and sampling plans for Diaphorina citri (Hemiptera: Psyllidae) in citrus. J Econ Entomol 101:1478–1487

    Article  PubMed  Google Scholar 

  • 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 46:511–515

    Article  CAS  PubMed  Google Scholar 

  • 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 63:4060–4067

    Article  CAS  PubMed  Google Scholar 

  • Stewart-Jones A, Poppy GM (2006) Comparison of glass vessels and plastic bags for enclosing living plant parts for headspace analysis. J Chem Ecol 32:845–864

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2014) R: A language and environment for statistical computing. Vienna. Available: http://www.R-project.org/

  • 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 6:536–543

    Google Scholar 

  • 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 19:173–179

    Article  CAS  Google Scholar 

  • Tiwari S, Sayed RS, Sayed ME, Stelinski LL (2011) Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Manag Sci 67:1258–1268

    Article  CAS  PubMed  Google Scholar 

  • Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671

    Article  CAS  PubMed  Google Scholar 

  • Tsagkarakis EA, Rogers ME (2010) Suitability of ‘Cleopatra’ mandarin as a host plant for Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 93:451–453

    Article  Google Scholar 

  • 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 2:15–19

    Google Scholar 

  • 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 36:1006–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 36:343–348

    Article  CAS  Google Scholar 

  • Wenninger EJ, Hall DG (2007) Daily timing of mating and age at reproductive maturity in Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 90:715–722

    Article  Google Scholar 

  • 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 38:225–234

    Article  PubMed  Google Scholar 

  • Westbrook CJ, Hall DG, Stover E, Duan YP, Lee RF (2011) Colonization of citrus and citrus-related germplasm by Diaphorina citri (Hemiptera: Psyllidae). HortScience 46:997–1005

    Google Scholar 

  • Yamamoto PT, Bassanezi RB (2003) Seletividade de produtos fitossanitários aos inimigos naturais de pragas dos citros. Laranja 24:353–382

    Google Scholar 

  • Yamamoto PT, Alves GR, Beloti VH (2014) Manejo e controle do huanglongbing (HLB) dos cítricos. Investig Agrar 16:69–82

    Google Scholar 

  • 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 17:35–45

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Entomology and Acarology, ‘Luiz de Queiroz’ College of Agriculture/University of São Paulo (ESALQ/USP), Piracicaba, São Paulo, 13418-900, Brazil

    V. H. Beloti, F. Santos, G. R. Alves, J. M. S. Bento & P. T. Yamamoto

Authors
  1. V. H. Beloti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. R. Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. M. S. Bento
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. T. Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. H. Beloti.

Additional information

Handling Editor: Anna-Karin Borg-Karlson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 45 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beloti, V.H., Santos, F., Alves, G.R. et al. Curry leaf smells better than citrus to females of Diaphorina citri (Hemiptera: Liviidae). Arthropod-Plant Interactions 11, 709–716 (2017). https://doi.org/10.1007/s11829-017-9524-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-017-9524-6

Keywords

Search

Navigation