Journal of Insect Behavior

, Volume 31, Issue 3, pp 298–308 | Cite as

Trail Chemicals of the Convergens Ladybird Beetle, Hippodamia convergens, Reduce Feeding and Oviposition by Diaphorina citri (Hemiptera: Psyllidae) on Citrus Plants

  • Meeja Seo
  • Monique J. Rivera
  • Lukasz L. Stelinski


We investigated feeding and oviposition behavior of the Asian citrus psyllid, Diaphorina citri, when exposed to the foraging trails of the convergens ladybird beetle, Hippodamia convergens. Diaphorina citri females feeding on citrus leaves directly exposed to the ladybird adults or treated with trail extract excreted significantly less honeydew droplets than controls. The trail chemicals of the ladybird beetle also decreased oviposition by D. citri females on citrus. In a no-choice experiment, D. citri females preferred to oviposit on control flush and plants than those with ladybird trail-extract treatments. In two-choice experiments, 68.0% of D. citri released into cages exhibited strong selection preference for settling and eventual oviposition on control plants than plants treated with ladybird trail extract. Diaphorina citri eggs were found on all new leaf flush of control plants, whereas only 29.5% of flush on treatment plants were selected for oviposition. The trail chemical deposited by the convergens ladybird beetle elicits repellency of D. citri feeding and oviposition. Therefore, the trail chemicals my contain components that could be useful for behavior-based management of D. citri and HLB disease by reducing psyllid feeding and oviposition.


Hippodamia convergens Coccinellidae huanglongbing (HLB) feeding inhibition oviposition inhibition Diaphorini citri 



We thank Wendy L. Meyer, Angelique B. Hoyte, Kristin A. Racine, and Hunter Gossett for technical support. We really appreciate Timothy A. Ebert for giving the pea aphid for rearing ladybird beetles. This project was supported by the Citrus Research and Development Foundation grant number 15-024.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.


  1. Ammar ED, Ramos JE, Hall DG, Dawson WO, Shatters RG (2016) Acquisition, replication and inoculation of Candidatus Liberibacter asiaticus following various acquisition periods on huanglongbing-infected citrus by nymphs and adults of the Asian citrus psyllid. PLoS One 11(7):e0159594. CrossRefPubMedCentralGoogle Scholar
  2. Boina DR, Onagbola EO, Salyani M, Stelinski LL (2009) Antifeedant and sublethal effects of imidacloprid on Asian citrus psyllid, Diaphorina citri. Pest Manag Sci 65:870–877CrossRefPubMedGoogle Scholar
  3. Bové JM (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J Plant Pathol 88:7–37Google Scholar
  4. Crabtree RH (1985) The organometallic chemistry of alkanes. Chem Rev 85:245–269CrossRefGoogle Scholar
  5. Dixon AFG, Hemptinne JL, Kindlmann P (1997) Effectiveness of ladybirds as biological control agents: patterns and processes. Entomophaga 42:72–83CrossRefGoogle Scholar
  6. Doumbia M, Hemptinne JL, Dixon AFG (1998) Assessment of patch quality of ladybird: role of larval tracks. Oecologia 113:197–202CrossRefPubMedGoogle Scholar
  7. Ferrero D, Lemon J, Fluegge D, Pashkovski S, Korzan W, Datta S, Fendt M, Liberles S (2001) Detection and avoidance of a carnivore odor by prey. Proc R Soc B Biol Sci 108:11235–11240Google Scholar
  8. George J, Ammar ED, Hall DG, Lapointe SL (2017) Sclerenchymatous ring as a barrier to phloem feeding by Asian citrus psyllid: evidence from electrical penetration graph and visualization of stylet pathways. PLoS One 12:e0173520. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Gottwald TR (2010) Current epidemiological understanding of citrus huanglongbing. Annu Rev Phytopathol 48:119–139CrossRefPubMedGoogle Scholar
  10. Grafton-Cardwell E, Stelinski LL, Stansly PA (2013) Biology and management of Asian citrus psyllid, vector of huanglongbing pathogens. Annu Rev Entomol 58:413–432CrossRefPubMedGoogle Scholar
  11. Hall DG, Richardson ML, Ammar ED, Halbert SE (2013) Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae), vector of citrus huanglongbing disease. Entomol Exp Appl 146:207–223CrossRefGoogle Scholar
  12. Hemptinne JL, Dixon AFG (1991) Why ladybird have generally been so ineffective in biological control? In: Polgar L, Chambers RJ, Dixon AFG, Hodek I (eds) Behavior and impact of Aphidophag. SPB Academic Publishing, The Hague, pp 149–157Google Scholar
  13. Hemptinne JL, Lognay G, Doumbia M, Dixon AFG (2001) Chemical nature and persistence of the oviposition deterring pheromone in the tracks of the larvae of the two spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Chemoecology 11:43–47CrossRefGoogle Scholar
  14. Inoue H, Ohnishi J, Ito T, Tomimura K, Miyata S, Iwanami T (2009) Enhanced proliferation and efficient transmission of Candidatus Liberibacter asiaticus by adult Diaphorina citri after acquisition feeding in the nymphal stage. Ann Appl Biol 155:29–36CrossRefGoogle Scholar
  15. Magro A, Tene JN, Bastin N, Dixon AFG, Hemptinne JL (2007) Assessment of patch quality by ladybirds: relative response to conspecific and heterospecific larval tracks a consequence of habitat similarity? Chemoecology 17:37–45CrossRefGoogle Scholar
  16. Martini X, Dixon AFG, Hemptinne JL (2013) The effect of relatedness on the response of Adalia bipunctata L. to oviposition deterring cues. Bull Entomol Res 103:14–19CrossRefPubMedGoogle Scholar
  17. Martini X, Kuhus EH, Hoyte A, Stelinski LL (2014) Plant volatiles and density-dependent conspecific female odors are used by Asian citrus psyllid to evaluate host specific suitability on a spatial scale. Arthropod Plant Interact 8:453–460CrossRefGoogle Scholar
  18. Michaud JP (2001) Numerical response of Olla v-nigram (Mulsant)(Coleoptera: Coccinellidae) to infestations of Asian citrus psyllid (Hemiptera: Psyllidae) in Florida. Fla Entomol 84:608–612CrossRefGoogle Scholar
  19. Michaud J.P. 2004. Natural mortality of asian citrus psyllid (Homoptera: Psyllidae) in Central Florida. Biol. Control. 29:260-269.Google Scholar
  20. Michaud JP, Olsen LE (2004) Suitability of Asian citrus psyllid, Diaphorina citri, as prey for ladybeetles. BioControl 49:417–431CrossRefGoogle Scholar
  21. Mowry TM, Ophus JD (2002) Effects of sub-lethal imidacloprid levels on potato leafroll virus transmission by Myzus persicae. Entomol Exp Appl 103:249–255CrossRefGoogle Scholar
  22. Nakashima Y, Birkett MA, Pye BJ, Pickett JA, Powell W (2004) The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae) by the aphid parasitoids, Aphidius ervi (Hymenoptera: Braconidae). J Chem Ecol 30:1103–1115CrossRefPubMedGoogle Scholar
  23. Nauen R (1995) Behaviour-modifying effects of low systemic concentrations of imidaclorid on Myzus persicae with species reference to an antifeeding response. Pestic Sci 44:145–153CrossRefGoogle Scholar
  24. Nauen R, Elbert A (1997) Apparent tolerance of a field-collected strain of Myzus nicotianae to imidacloprid due to strong antifeedant responses. Pestic Sci 49:252–258CrossRefGoogle Scholar
  25. Ninkovic V, Feng Y, Olsson U, Petterson J (2013) Ladybird footprints induce aphid avoidance behavior. Biol Control 65:63–71CrossRefGoogle Scholar
  26. Oliver TH, Jones I, Cook JM, Leather SR (2008) Avoidance responses of an aphidophagous ladybird Adalia bipunctata, to aphid-tending ants. Ecol Entomol 33:523–528CrossRefGoogle Scholar
  27. Patt JM, Sétamou M (2010) Responses of the Asian citrus psyllids, Diaphorina citri (Hemiptera: Psyllidae), to volatiles emitted by the flushing shoots of its rutaceous host plants. Environ Entomol 39:618–624CrossRefPubMedGoogle Scholar
  28. Patt J.M., Meikle W.G., Mafra-Neto A., Setamou M., Mangan R., Yang C., Malik N., Adamczyk J.J. 2001. Multimodal cues drive host-plant assessment in Asian citrus psyllid (Diaphorina citri). Environ Entomol 40:1494–1502.Google Scholar
  29. Pelz-Stelinski KS, Brlansky RH, Ebert TA, Rogers ME (2010) Transmissoin parameters for Candidatus Liberibacter asiaticus by Asian citrus psyllid (Hemiptera: Psyllidae). J Econ Entomol 103:1531–1541CrossRefPubMedGoogle Scholar
  30. Roistacher CN (1991) Techniques for biological detection of specific graft transmissible diseases, in Graft-transmissible diseases of Citrus. In: Roistacher CN (ed) Food and agricultural organization. Rome, Italy, p 35–45Google Scholar
  31. Seo M, Rivera MJ, Stelinski LL, Martini X (2018) Ladybird beetle trails reduce host acceptance by Diaphorina citri Kuwayama (Hemiptera: Leviidae). Biol Control 121:30–35CrossRefGoogle Scholar
  32. Sétamou M, da Graca JV, Sandoval JL (2016) Suitability of native American Rutaceae to serve as host plants for the Asian citrus psyllid (Hemiptera: Liviidae). J Appl Entomol 140:645–654CrossRefGoogle Scholar
  33. Swihart RK, Pignatello JJ, Mattina MIJ (1991) Aversive response of white-tailed deer, Odocoileus virgonianus, to predator urines. J Chem Ecol 17:767–777CrossRefPubMedGoogle Scholar
  34. Tiwari S, Mann RS, Rogers ME, Stelinski LL (2011) Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Manag Sci 67:1258–1268CrossRefPubMedGoogle Scholar
  35. Tiwari S, Clayson PJ, Kyhns EE, Stelinski LL (2012) Effects of buprofezin and diflubenzuron on various developmental stages of Asian citrus psyllid, Diaphorina citri. Pest Manag Sci 68:1405–1412CrossRefPubMedGoogle Scholar
  36. Wenniger EJ, Hall DG (2007) Daily timing of mating and age at reproductive maturity in Diaphorina citri (Hemiptera: psyllidae). Fla Entomol 90:715–722CrossRefGoogle Scholar
  37. Wenninger EJ, Stelinski LL, Hall DG (2009) Roles of olfactoty 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
  38. Wheeler CA, Cardé RT (2013) Defensive allomones function as aggregation pheromones in diapausing ladybird beetles, Hippodamia convergens. J Chem Ecol 39:723–732CrossRefPubMedGoogle Scholar
  39. Wheeler CA, Cardé RT (2014) Following in their footprints: cuticular hydrocarbons as overwintering aggregation site markers in Hippodamia convergens. J Chem Ecol 40:418–428CrossRefPubMedGoogle Scholar
  40. Wheeler CA, Millar JG, Cardé RT (2015) Multimodal signal interactions in the ladybeetle, Hippodamia convergens, aposematic system. Chemoecology 25:123–133CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Entomology and Nematology Department, Citrus Research and Education CenterUniversity of FloridaLake AlfredUSA

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