Efficiency of plant induced volatiles in attracting Encarsia formosa and Serangium japonicum, two dominant natural enemies of whitefly Bemisia tabaci in China

Pest Management Science

Volumn 70, Issue 10, 2014, Pages 1604-1610

  Li, Shao Jian ^a   Ren, Su Li ^a   Xue, Xia ^a   Ren, Shun Xiang ^a   Cuthbertson, Andrew G S ^b   van Dam, Nicole M ^c   Qiu, Bao Li ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b FOOD AND ENVIRONMENT RESEARCH AGENCY   (United Kingdom)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Bemisia tabaci; Biological control; Foraging behaviour; Natural enemy; Plant volatile

Indexed keywords

ALEYRODIDAE; BEMISIA TABACI; BRASSICA OLERACEA VAR. ITALICA; ENCARSIA FORMOSA; SERANGIUM;

CYCLOPENTANE DERIVATIVE; JASMONIC ACID; OXYLIPIN; PHYTOHORMONE;

ANIMAL; BEETLE; BIOLOGICAL PEST CONTROL; BRASSICA; CHEMISTRY; CHINA; FEMALE; HEMIPTERA; HERBIVORY; HYMENOPTERA; ODOR; PARASITOLOGY; PHYSIOLOGY; PROCEDURES;

ANIMALS; BEETLES; BRASSICA; CHINA; CYCLOPENTANES; FEMALE; HEMIPTERA; HERBIVORY; HYMENOPTERA; ODORS; OXYLIPINS; PEST CONTROL, BIOLOGICAL; PLANT GROWTH REGULATORS;

EID: 84925233166     PISSN: 1526498X     EISSN: 15264998     Source Type: Journal    
DOI: 10.1002/ps.3749     Document Type: Article

References (56)

1. Vet LEM and Dicke M, Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141-172 (1992).
2. Langley SA, Tilmon KJ, Cardinale BJ and Ives AR, Learning by the parasitoid wasp, Aphidius ervi (Hymenoptera:Braconidae), alters individual fixed preferences for pea aphid color morphs. Oecologia 150:172-179 (2006).
3. Vet LEM and Groenewold AW, Semiochemicals and learning in parasitoids. J Chem Ecol 16:3119-3135 (1990).
4. Papaj DR and Vet LEM, Odor learning and foraging success in the parasitoid, Leptopilina heterotoma. J Chem Ecol 16:3137-3150 (1990).
5. Bleeker MAK, Smid HM, Steidle JLM, Kruidhof HM, Van Loon JJA and Vet LEM, Differences in memory dynamics between two closely related parasitoid wasp species. Anim Behav 71:1343-1350 (2006).
6. Vet LEM, Evolutionary aspects of plant-carnivore interactions, in Insect-Plant Interactions and Induced Plant Defence, ed. by Chadwick DJ and Goode J. John Wiley & Sons, Ltd, Chichester, UK, pp. 3-20 (1999).
7. Mumm R, Posthumus MA and Dicke M, Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant Cell Environ 31:575-585 (2008).
8. Vet LEM, Wackers FL and Dicke M, How to hunt for hiding hosts - the reliability-detectability problem in foraging parasitoids. Neth J Zool 41:202-213 (1991).
9. Tumlinson JH, Turlings TCJ and Lewis WJ, Semiochemically mediated foraging behaviour in beneficial parasitic insects. Arch Insect Biochem 22:385-391 (1993).
10. Turlings TCJ and Benrey B, Effects of plant metabolites on the behaviour and development of parasitic wasps. Ecoscience 5:321-333 (1998).
11. Dudareva N, Negre F, Nagegowda DA and Orlova I, Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417-440 (2006).
12. Hilker M and Meiners T, Early herbivore alert: insect eggs induce plant defense. J Chem Ecol 32:1379-1397 (2006).
13. Mumm R and Hilker M, Direct and indirect chemical defence of pine against folivorous insects. Trends Plant Sci 11:351-358 (2006).
14. Soler R, Harvey JA, Kamp AFD, Vet LEM, van der Putten WH, van Dam NM et al., Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos 116:367-376 (2007).
15. van Dam NM and Oomen MWAT, Root and shoot jasmonic acid applications differentially affect leaf chemistry and herbivore growth. Plant Signal Behav 3:91-98 (2008).
16. Qiu BL, Harvey JA, Raaijmakers CE, Vet LEM and van Dam NM, Non-linear effects of plant root and shoot jasmonic acid application on the performance of Pieris brassicae and its parasitoid Cotesia glomerata. Funct Ecol 23:496-505 (2009).
17. Bargmann CI, Comparative chemosensation from receptors to ecology. Nature 444:295-301 (2006).
18. Mumm R and Hilker M, The significance of background odour for an egg parasitoid to detect plants with host eggs. Chem Senses 30:337-343 (2005).
19. van Dam NM, Qiu BL, Hordijk CA, Vet LEM and Jansen JJ, Identification of biologically relevant compounds in aboveground and belowground induced volatile blends. J Chem Ecol 36:1006-1016 (2010).
20. De Barro PJ, Liu SS, Boykin LM and Dinsdale AB, Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1-19 (2011).
21. Cock MJW, Bemisia tabaci - a Literature Survey on the Cotton Whitefly with an Annotated Bibliography. CAB International Institute of Biological Control, Ascot, UK, 121 pp. (1986).
22. Oliveira MRV, Henneberry TJ and Anderson P, History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot 20:709-723 (2001).
23. Estrada-Hernandez MG, Valenzuela-Soto JH, Ibarra-Laclette E and Delano-Frier JP, Differential gene expression in whitefly Bemisia tabaci-infested tomato (Solanum lycopersicum) plants at progressing developmental stages of the insect's life cycle. Physiol Plant 137:44-60 (2009).
24. Brown JK and Czosnek H, Whitefly transmission of plant viruses. Adv Bot Res 36:65-76 (2002).
25. Jones DR, Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109:195-219 (2003).
26. Polaszek A, Evans GA and Bennett FA, Encarsia parasitoids of Bemisia tabaci (Hymenoptera: Aphelinidae, Homoptera: Aleyrodidae). A preliminary guide to identification. Bull Entomol Res 82:375-392 (1992).
27. Hoddle MS, Van Driesche RG, Sanderson JP and Minkenberg OPJM, Biological control of Bemisia argentifolii (Hemiptera: Aleyrodidae) on poinsettia with inundative releases of Eretmocerus eremicus (Hymenoptera: Aphelinidae): do release rates affect parasitism? Bull Entomol Res 88:47-58 (1998).
28. Jiang YX, de Blas C, Barrios L and Fereres A, Correlation between whitefly (Homoptera: Aleyrodidae) feeding behaviour and transmission of tomato yellow leaf curl virus. Ann Entomol Soc Am 93:573-579 (2000).
29. van Lenteren JC, Cock MJW, Hoffmeister TS and Sands DPA, Host ranges of natural enemies as an indicator of non-target risk. 2nd Int Symp - Biological Control of Arthropods, Davos, Switzerland, pp. 584-592 (2005).
30. Pang ST, Wang L, Hou YH and Shi ZH, Interspecific interference competition between Encarsia formosa and Encarsia sophia (Hymenoptera: Aphelinidae) in parasitizing Bemisia tabaci (Hemiptera: Aleyrodidae) on five tomato varieties. Insect Sci 18:92-100 (2011).
31. Yao SL, Ren SX and Huang Z, The morphological characters and biology of Serangium japonicum. Nat Enemies Insects 26:22-27 (2004).
32. He YX, Zhao JW, Zheng Y, Desneux N and Wu KM, Lethal effect of imidacloprid on the coccinellid predator Serangium japonicum and sublethal effects on predator voracity and on functional response to the whitefly Bemisia tabaci. Ecotoxicology 21:1291-1300 (2012).
33. Moore JP, Paul ND, Whittaker JB and Taylor JE, Exogenous jasmonic acid mimics herbivore-induced systemic increase in cell wall bound peroxidase activity and reduction in leaf expansion. Funct Ecol 17:549-554 (2003).
34. Kessler A and Baldwin IT, Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141-2144 (2001).
35. Thaler JS, Stout MJ, Karban R and Duffey SS, Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol Entomol 26:312-324 (2001).
36. Qiu BL, van Dam NM, Harvey JA and Vet LEM, Root and shoot jasmonic acid induction differently affects the foraging behaviour of Cotesia glomerata under semi-field conditions. BioControl 57:387-395 (2012).
37. Vet LEM, van Lenteren JC, Heymans M and Meelis E, An air flow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiol Entomol 8:97-106 (1983).
38. ® 9.2. User'9 Guide. SAS Institute Inc., Cary, NC (2008).
39. Cuthbertson AGS and Murchie AK, European red spider mite - an environmental consequence of persistent chemical pesticide application. Int J Environ Sci Technol 2:287-290 (2005).
40. Poppy GM, Powell W and Pennacchio F, Aphid parasitoid responses to semiochemicals - genetic, conditioned or learnt? Entomophaga 42:193-199 (1997).
41. Francis F, Lognay G and Haubruge E, Olfactory responses to aphid and host plant volatile releases: (E)-beta-farnesene - an effective kairomone for the predator Adalia bipunctata. J Chem Ecol 30:741-755 (2004).
42. Zarate SI, Kempema LA and Walling LL, Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866-875 (2007).
43. Zhang PJ, Li WD, Huang F, Zhang JM, Xu FC and Lu YB, Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting salicylic acid signaling. J Chem Ecol 39:612-619 (2013).
44. Elbaz M, Halon E, Malka O, Malitsky S, Blum E, Aharoni A et al., Asymmetric adaptation to indolic and aliphatic glucosinolates in the B and Q sibling species of Bemisia tabaci (Hemiptera: Aleyrodidae). Mol Ecol 21:4533-4546 (2012).
45. Zhang PJ, Broekgaarden C, Zheng SJ, Snoeren TAL, van Loon JJA, Gols R et al., Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol 197:1291-1299 (2013).
46. Li SJ, Xue X, Ren SX, Cuthbertson AGS, van Dam NM and Qiu B-L, Root and shoot jasmonic acid induced plants differently affect the performance of Bemisia tabaci and its parasitoid Encarsia formosa. Basic Appl Ecol 14:670-679 (2013).
47. Zhang PJ, Xu CX, Zhang JM, Lu YB, Wei JN, Liu YQ et al., Phloem-feeding whiteflies can fool their host plants, but not their parasitoids. Functional Ecol 27:1304-1312 (2013).
48. Zhu JW, Cossé AA, Obrycki JJ, Boo KS and Baker TC, Olfactory reactions of the twelve-spotted lady beetle, Coleomegilla maculata, and the green lacewing, Chrysoperla carnea, to semiochemicals released from their prey and host plant: electroantennogram and behavioral responses. J Chem Ecol 25:1163-1177 (1999).
49. Al Abassi S, Birkett MA, Pettersson J, Pickett JA, Wadhams LJ and Woodcock CM, Response of the seven-spot ladybird to an aphid alarm pheromone and an alarm pheromone inhibitor is mediated by paired olfactory cells. J Chem Ecol 26:1765-1771 (2000).
50. Ninkovic V, Al Abassi S and Pettersson J, The influence of aphid-produced plant volatiles on ladybird beetle searching behaviour. Biol Control 21:191-195 (2001).
51. Han B and Chen Z, Behavioural and electrophysiological responses of natural enemies to synomones from tea shoots and kairomones from tea aphids, Toxoptera aurantii. J Chem Ecol 28:2203-2220 (2002).
52. Zhang PJ, Van Loon JJA, Zheng S and Dicke M, Herbivore-induced volatiles of cabbage (Brassica oleracea) prime defence responses in neighbouring intact plants. Plant Biol 13:276-284 (2011).
53. van Dam NM, Witjes L and Svatos A, Interactions between aboveground and belowground induction of glucosinolates in two wild Brassica species. New Phytol 161:801-810 (2004).
54. van Dam NM and Raaijmakers CE, Local and systemic induced responses to cabbage root fly larvae (Delia radicum) in Brassica nigra and B. oleracea. Chemoecology 16:17-24 (2006).
55. Mithen RF, Lewis BG, Heaney RK and Fenwick GR, Resistance of leaves of Brassica species to Leptosphaeria maculans. Trans Br Mycol Soc 88:525-531 (1987).
56. van Dam NM, Harvey JA, Wäckers FL, Bezemer TM, van der Putten WH and Vet LEM, Interactions between aboveground and belowground induced responses. Basic Appl Ecol 4:63-77 (2003).