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A female attractant for the blue gum chalcid, Leptocybe invasa (Hymenoptera: Eulophidae), from host plant (DH 201-2: Eucalyptus grandis × Eucalyptus tereticornis)

  • Tao Ma
  • Laijiao Lan
  • Na Lin
  • Lifei Zheng
  • Zhaohui Sun
  • Yizhen Li
  • Xiujun WenEmail author
Original Paper
  • 11 Downloads

Abstract

The blue gum chalcid, Leptocybe invasa, is a severe insect pest of Eucalyptus trees leading to gall formation, stunting, leaf deformation, and death in cases, China. In the previous studies, we found that the Eucalyptus hybrid, DH 201-2 (Eucalyptus grandis × Eucalyptus tereticornis), is highly preferred to L. invasa larvae and adults, but its mechanism has not been fully understood. In the present study, we investigated the volatile organic compounds (VOCs) from DH 201-2 that attract L. invasa. Volatiles were collected from fresh young leaves and identified with gas chromatography–mass spectrometry (GC–MS) and gas chromatography–electroantennogram detection (GC–EAD). The attraction of identified volatiles to L. invasa was then measured under laboratory and field conditions. Two EAD-active compounds, gamma-terpinene and Limonene, were identified. In the dose–response experiments, we found that the EAG response to L. invasa was enhanced with the increased concentration of EAD-active compounds, and gamma-terpinene showed the stronger EAG response than Limonene. Both four-arm olfactometer bioassays and field studies showed that the blend of gamma-terpinene and Limonene with a ratio of 8:2 significantly attracted more L. invasa as compared to other ratios. The potential use of these compounds in the control of L. invasa is ulteriorly discussed.

Keywords

Leptocybe invasa Volatile organic compounds (VOCs) Identification Four-arm olfactometer Field test 

Notes

Acknowledgements

The authors heartily thank anonymous reviewer for critical reading and valuable comments. This study was financed by research grant from the National Natural Science Foundation of China (No. 31600516) and the National Science and Technology Pillar Program during the 12th Five-year Plan Period (No. 2015BAD07B06-8).

References

  1. Abagale SA, Woodcock CM, Chamberlain K, Osafo-Acquaah S, van Emden H, Birkett MA, Pickett JA, Braimah H (2018) Attractiveness of host banana leaf materials to the banana weevil, Cosmopolites sordidus in Ghana for development of field management strategies. Pest Manag Sci.  https://doi.org/10.1002/ps.5182 Google Scholar
  2. Alemu MM (2016) Eucalyptus tree production in Wolayita Sodo, Southern Ethiopia. OAlib J 3:e3280Google Scholar
  3. Alhmedi A, Haubruge E, Francis F (2010) Identification of limonene as a potential kairomone of the harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 107:541–548CrossRefGoogle Scholar
  4. Anfora G, Tasin M, Cristofaro AD, Ioriatti C, Lucchi A (2009) Synthetic grape volatiles attract mated Lobesia botrana females in laboratory and field bioassays. J Chem Ecol 35:1054–1062CrossRefGoogle Scholar
  5. Angioy AM, Desogus A, Barbarossa IT, Erson P, Hansson BS (2003) Extreme sensitivity in an olfactory system. Chem Senses 28:279–284CrossRefGoogle Scholar
  6. Anton S, Dufour MC, Gadenne C (2007) Plasticity of olfactory-guided behavior and its neurobiological basis: lessons from moths to locusts. Entomol Exp Appl 123:1–11CrossRefGoogle Scholar
  7. Aytar F (2006) Natural history, distribution and hosts of Eucalyptus gall wasps in Turkey. VIII the European Congress of Entomology. In: 2006, Abstract book, PP4-25 (Poster Number) Poster Presentation. p. 156, Izmir, Turkey, on September 17–22Google Scholar
  8. Basavana Goud K, Kavitha Kumar N, Vastrad AS, Bhadragoudar M, Kulkarni HD (2010) Screening eucalyptus clones against Leptocybe invasa Fisher and La Salle (Hymenoptera: Eulophidae). Karnataka J Agric Sci 23:213–214Google Scholar
  9. Borges ED, Martins CB, da Silva RR, Zarbin PHG (2018) Terpenoids dominate the bouquet of volatile organic compounds produced by Passiflora edulis in response to herbivory by Heliconius erato phyllis (Lepidoptera: Nymphalidae). Arthropod-Plant Interact 12:123–131CrossRefGoogle Scholar
  10. Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274CrossRefGoogle Scholar
  11. Cha DH, Nojima S, Hesler SP, Zhang AJ, Linn CE Jr, Roelofs WL, Loeb GM (2008) Identification and field evaluation of grape shoot volatiles attractive to female grape berry moth (Paralobesia viteana). J Chem Ecol 34:1180–1189CrossRefGoogle Scholar
  12. Chen C, Song QS (2008) Responses of the pollinating wasp Ceratosolen solmsi marchali to odor variation between two floral stages of Ficus hispida. J Chem Ecol 34(12):1536–1544CrossRefGoogle Scholar
  13. Cossé AA, Endris JJ, Millar JG, Baker TC (1994) Identification of volatile compounds from fungus-infected date fruit that stimulate upwind flight in female Ectomyelois ceratoniae. Entomol Exp Appl 72:233–238CrossRefGoogle Scholar
  14. Dittrich-Schröder G, Wingfield MJ, Hurley BP, Slippers B (2012) Diversity in Eucalyptus susceptibility to the gall forming wasp Leptocybe invasa. Agr For Entomol 14:419–427CrossRefGoogle Scholar
  15. Doğanlar M, Hassan E (2010) Review of Australian species of Megastigmus (Hymenoptera: Torymidae) associated with Eucalyptus, with descriptions of new species. Aust J Basic Appl Sci 4:5059–5120Google Scholar
  16. FAO (1988) The eucalypt dilemma. FAO, Forestry Department, RomeGoogle Scholar
  17. Fatouros NE, Lucas-Barbosa D, Weldegergis BT, Pashalidou FG, van Loon JJA, Dicke M, Harvey JA, Gols R, Huigens ME (2012) Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS ONE 7(8):e43607CrossRefGoogle Scholar
  18. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414CrossRefGoogle Scholar
  19. Giron D, Dubreuil G, Bennett A, Dedeine F, Dicke M, Dyer LA, Erb M, Harris MO, Huguet E, Kaloshian I, Kawakita A, Lopez-Vaamonde C, Palmer TM, Petanidou T, Poulsen M, Sallé A, Simon J, Terblanche JS, Thiéry D, Whiteman NK, Woods HA, Pincebourde S (2018) Promises and challenges in insect-plant interactions. Entomol Exp Appl 166:319–343CrossRefGoogle Scholar
  20. Gothilf S, Levy E, Cooper R, Lavie D (1975) Oviposition stimulants of the moth Ectomyelois ceratoniae: the effect of short-chain alcohols. J Chem Ecol 1:457–464CrossRefGoogle Scholar
  21. Grattapaglia D, Vaillancourt RE, Shepherd M, Thumma BR, Foley W, Külheim C, Potts BM, Myburg AA (2012) Progress in Myrtaceae genetics and genomics: Eucalyptus as the pivotal genus. Tree Genet Genomics 8:463–508CrossRefGoogle Scholar
  22. Hern A, Dorn S (2004) A female-specific attractant for the codling moth, Cydia pomonella, from apple fruit volatiles. Naturwissenschaften 91:77–80CrossRefGoogle Scholar
  23. Hosseini SA, Goldansaz SH, Menken SBJ, van Wijk M, Roessingh P, Groot AT (2017) Field attraction of carob moth to host plants and conspecific females. J Econ Entomol 110:2076–2083CrossRefGoogle Scholar
  24. Huang YH, Zhang NN, He PL, Huang SB, Huang HH, Chen RB (2014) Resistance of different Eucalyptus strains to Leptocybe invasa Fisher & La Salle. Chin J Biol Control 30(3):316–322. (in Chinese)Google Scholar
  25. Kant MR, Bleeker PM, Van Wijk M, Schuurink RC, Harring MA (2009) Plant volatiles in defence. Adv Bot Res 51:613–666CrossRefGoogle Scholar
  26. Kim IK, Mendel Z, Protasov A, Blumberg D, La Salle J (2008) Taxonomy, biology and efficacy of two Australian parasitoids of the Eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae: Tetrastichinae). Zootaxa 1910:1–20Google Scholar
  27. Krishnakumar N, Jacob JP (2010) Eucalyptus gall—a recent invasive in man-modified forest ecosystem in Andhra Pradesh. Karnataka J Agric Sci 23:217–219Google Scholar
  28. Kulkarni H, Kumari NK, Vastrad AS, Basavanagoud K (2010) Release and recovery of parasitoids in eucalyptus against gall wasp, Leptocybe invasa (Hymenoptyera: Eulophidae) under green house. Karnataka J Agric Sci 23:91–92Google Scholar
  29. Landolt PJ, Guédot C (2008) Field attraction of codling moths (Lepidoptera: Tortricidae) to apple and pear fruit, and quantitation of kairomones from attractive fruit. Ann Entomol Soc Am 101:675–681CrossRefGoogle Scholar
  30. Lanfranco D, Dungey HS (2001) Insect damage in Eucalyptus: a review of plantations in Chile. Aust Ecol 26:477–481CrossRefGoogle Scholar
  31. Leather SR (1985) Oviposition preferences in relation to larval growth rates and surviva in the pine beauty moth, Panolis flammea. Ecol Entomol 10:213–217CrossRefGoogle Scholar
  32. Leather SR (1987) Pine monoterpenes stimulate oviposition in the pine beauty moth, Panolis flammea. Entomol Exp Appl 43:295–303CrossRefGoogle Scholar
  33. Linn CE, Dambroski H, Nojima S, Feder JL, Berlocher SH, Roelofs WL (2005) Variability in response specificity of apple, hawthorn, and flowering dogwood-infesting Rhagoletis flies to host fruit volatile blends: implications for sympatric host shifts. Entomol Exp Appl 116:55–64CrossRefGoogle Scholar
  34. Ma T, Zheng LF, Yang XC, Zhu XJ, Zhang M, Li YZ, Wen XJ (2013) The chemotaxis of Leptocybe invasa to volatile substanes from different Eucalyptus. Chin For Sci Technol 27:123–125. (in Chinese)Google Scholar
  35. Mendel Z, Protasov A, Fisher N, La Salle J (2004) Taxonomy and biology of Leptocybe invasa gen. & sp. n. (Hymenoptera: Eulophidae), an invasive gall inducer on Eucalyptus. Aust J Entomol 43:101–113CrossRefGoogle Scholar
  36. Mewalal R, Rai DK, Kainer D, Chen F, Külheim C, Peter GF, Tuskan GA (2017) Plant-derived terpenes: a feedstock for specialty biofuels. Trends Biotechnol 35:227–240CrossRefGoogle Scholar
  37. Moore B, Andrew R, Külheim C, Foley W (2014) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol 201:733–750CrossRefGoogle Scholar
  38. Naidoo S, Christie N, Acosta JJ, Mphahlele MM, Payn KG, Myburg AA, Külheim C (2018) Terpenes associate with resistance against the gall wasp, Leptocybe invasa, in Eucalyptus grandis. Plant Cell Environ 41:1840–1851CrossRefGoogle Scholar
  39. Nyeko P, Mutitu EK, Day RK (2009) Eucalyptus infestation by Leptocybe invasa in Uganda. Afr J Ecol 47:299–307CrossRefGoogle Scholar
  40. Oates CN, Külheim C, Myburg AA, Slippers B, Naidoo S (2015) The transcriptome and terpene profile of Eucalyptus grandis reveals mechanisms of defense against the insect pest Leptocybe invasa. Plant Cell Physiol 56(7):1418–1428CrossRefGoogle Scholar
  41. Padovan A, Keszei A, Külheim C, Foley WJ (2013) The evolution of foliar terpene diversity in Myrtaceae. Phytochem Rev 13:695–716CrossRefGoogle Scholar
  42. Piñero JC, Dorn S (2009) Response of female oriental fruit moth to volatiles from apple and peach trees at three phenological stages. Entomol Exp Appl 131:67–74CrossRefGoogle Scholar
  43. Pohjonen V, Pukkala T (1990) Eucalyptus globulus in Ethiopian forestry. Forest Ecol Manag 36:19–31CrossRefGoogle Scholar
  44. Protasov A, Doganlar M, La Salle J, Mendel Z (2008) Occurrence of two local Megastigmus species parasitic on the Eucalyptus gall wasp Leptocybe invasa in Israel and Turkey. Phytoparasitica 36:449–459CrossRefGoogle Scholar
  45. Ramadan HM (2004) Morphological characteristics and distribution of Aprostocetus sp. (Hymenoptera: Eulophidae: Tetrastichinae) a gall wasp of Eucalyptus new for Egypt. Alexandria J Agr Res 49:59–63Google Scholar
  46. Randlkofer B, Obermaier E, Hilker M, Meiners T (2010) Vegetation complexity-the influence of plant species diversity and plant structures on plant chemical complexity and arthropods. Basic Appl Ecol 5:383–395CrossRefGoogle Scholar
  47. Rawat V, Negi JD (2004) Biomass production of Eucalyptus tereticornis in different agroecological regions of India. Indian For 130(7):762–770Google Scholar
  48. Ruebenbauer A, Schlyter F, Hansson BS, Löfstedt C, Larsson MC (2008) Genetic variability and robustness of host odour preference in Drosophila melanogaster. Curr Biol 18:1438–1443CrossRefGoogle Scholar
  49. Sangtongpraow B, Charernsom K, Siripatanadilok S (2011) Longevity, fecundity and development time of Eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae) in Kanchanaburi Province, Thailand. Thai J Agric Sci 44:155–163Google Scholar
  50. Senthilkumar N, Thangapandian K, Murugesan S, Jacob JP, Krishnakumar N (2013) Invasive alien Eucalyptus gall wasp, Leptocybe invasa (Fisher and Lasalle): a threat to Eucalyptus plantations in Tamilnadu (India). Acad J Entomol 6:146–152Google Scholar
  51. Sexena N (1991) Marketing constraints for Eucalyptus from farm lands in India. Agrofor Syst 13:73–85CrossRefGoogle Scholar
  52. Shu S, Grant GG, Langevin D, Lombardo DA, Macdonald L (1997) Oviposition and electroantennogram responses of Dioryctria abietivorella (Lepidoptera: Pyralidae) elicited by monoterpenes and enantiomers from eastern white pine. J Chem Ecol 23:35–50CrossRefGoogle Scholar
  53. Tasin M, Backman AC, Bengtsson M, Ioriatti C, Witzgall P (2006) Essential host plant cues in the grapevine moth. Naturwissenschaften 93:141–144CrossRefGoogle Scholar
  54. Tasin M, Bäckman AC, Coracini M, Casado D, Ioriatti C, Witzgall P (2007) Synergism and redundancy in a plant volatile blend attracting grapevine moth females. Phytochemistry 68:203–209CrossRefGoogle Scholar
  55. Tasin M, Bäckman AC, Anfora G, Carlin S, Ioriatti C, Witzgall P (2009) Attraction of female grapevine moth to common and specific olfactory cues from 2 host plants. Chem Senses 35:57–64CrossRefGoogle Scholar
  56. Thu PQ, Dell B, Burgess TI (2009) Susceptibility of 18 eucalypt species to the gall wasp Leptocybe invasa in the nursery and young plantations in Vietnam. Sci Asia 35:113–117CrossRefGoogle Scholar
  57. Tooker JF, Crumrin AL, Hanks LM (2005) Plant volatiles are behavioral cues for adult females of the gall wasp Antistrophus rufus. Chemoecology 15:85–88CrossRefGoogle Scholar
  58. Turnbull JW (1999) Eucalyptus plantations. New For 17:37–52CrossRefGoogle Scholar
  59. Visser JH, Avé DA (1978) General green leaf volatiles in the olfactory orientation of the Colorado beetle, Leptinotarsa decemlineata. Entomol Exp Appl 24:738–749CrossRefGoogle Scholar
  60. Wu YJ, Jiang XJ, Li DW, Luo JT, Zhou GF, Chang MS, Yang ZQ (2009a) Leptocybe invasa, a new invasive forest pest making galls on twigs and leaves of Eucalyptus trees in China (Hymenoptera: Eulophidae). Sci Silvae Sin 45(7):161–163. (in Chinese)Google Scholar
  61. Wu YJ, Xi FS, Luo JT, Li DW, Chang MS (2009b) Biological characteristics of Leptocybe invasa and its control technology. Guangxi Plant Prot 22:5–8. (in Chinese)Google Scholar
  62. Wylie F, Speight R (2012) Insect pests in tropical forestry. CABI Publishing, WallingfordCrossRefGoogle Scholar
  63. Xu H, Turlings TCJ (2018) Plant volatiles as mate-finding cues for insects. Trends Plant Sci 23:100–111CrossRefGoogle Scholar
  64. Yang XC, Li YZ, Wen XJ, Cao Y, Zheng LF, Cao CL, Ma T, Zhang M, Zhu XJ, Yi SY (2014) Preparation and controlled release effectiveness of microcapsules volatile oil from Eucalyptus. Chin J Biol Control 30(4):472–480. (in Chinese)Google Scholar
  65. Zakir A, Sadek MM, Bengtsson M, Hansson BS, Witzgall P, Anderson P (2013) Herbivore-induced plant volatiles provide associational resistance against an ovipositing herbivore. J Ecol 101:410–417CrossRefGoogle Scholar
  66. Zhang ZD (2008) A review on development situation and sustainable management of Eucalypt plantation. Sci Silvae Sin 44(7):97–102. (in Chinese)Google Scholar
  67. Zhu FL, Qiu BL, Ren SX (2013) The continuous life-table of Leptocybe invasa. Acta Ecol Sin 33:97–102. (in Chinese)CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape ArchitectureSouth China Agricultural UniversityGuangzhouChina

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