Differential Performance and Parasitism of Caterpillars on Maize Inbred Lines with Distinctly Different Herbivore-Induced Volatile Emissions

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Degen, Thomas ^a   Bakalovic, Nenad ^a   Bergvinson, David ^b,c   Turlings, Ted C J ^a  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^b Centro International de Mejoramiento de Maíz y Trigo CIMMYT   (Mexico)

^c BILL AND MELINDA GATES FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HEXENAL; BERGAMOTTIN; BETA FARNESENE; BOURBONENE; CARYOPHYLLENE; COPAENE; GERANYL ACETATE; INDOLE; LIMONENE; LINALOOL; MYRCENE; OCIMENE; PINENE; SALICYLIC ACID METHYL ESTER; SESQUITERPENE; VOLATILE AGENT; ZINGIBERENE;

ARTICLE; CAMPOLETIS SONORENSIS; CATERPILLAR; CONTROLLED STUDY; COTESIA MARGINIVENTRIS; DRY WEIGHT; HERBIVORE; INBRED STRAIN; INFESTATION; LABORATORY TEST; LARVA; MAIZE; MYCOPARASITISM; NOCTUIDAE; NONHUMAN; PARASITOID; PEST CONTROL; PLANT LEAF; PREDATOR; SPODOPTERA FRUGIPERDA; SURVIVAL RATE; WASP;

ANIMALS; HERBIVORY; HOST-PARASITE INTERACTIONS; ODORS; SPODOPTERA; VOLATILIZATION; ZEA MAYS;

CAMPOLETIS SONORENSIS; COTESIA MARGINIVENTRIS; HEXAPODA; SPODOPTERA FRUGIPERDA; VESPOIDEA; ZEA MAYS;

EID: 84868130696     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047589     Document Type: Article

References (57)

1. Dicke M, Baldwin IT, (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'. Trends Plant Sci 15: 167-175.
2. Turlings TCJ, Wäckers F (2004) Recruitment of predators and parasitoids by herbivore-injured plants. In: Cardé RT, Millar JG, editors. Advances in Insect Chemical Ecology: Cambridge University Press.
3. Kessler A, Baldwin IT, (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291: 2141-2144.
4. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH, (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393: 570-573.
5. Thaler JS, (1999) Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399: 686-688.
6. Faeth SH, editor (1994) Induced plant responses: effects on parasitoids and other natural enemies of phytophagous insects. Oxford: Oxford University Press. 245-260 p.
7. van der Meijden E, Klinkhamer PGL, (2000) Conflicting interests of plants and the natural enemies of herbivores. Oikos 89: 202-208.
8. Allison JD, Hare JD, (2009) Learned and naïve natural enemy responses and the interpretation of volatile organic compounds as cues or signals. New Phytol 184: 768-782.
9. Agrawal AA, (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25: 420-432.
10. Hare JD, (2011) Ecological Role of Volatiles Produced by Plants in Response to Damage by Herbivorous Insects. Annu Rev Entomol 56: 161-180.
11. Kessler A, Heil M, (2011) The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25: 348-357.
12. Turlings TCJ, Tumlinson JH, Lewis WJ, (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250: 1251-1253.
13. Bernasconi Ockroy ML, Turlings TCJ, Edwards PJ, Fritzsche-Hoballah ME, Ambrosetti L, et al. (2001) Response of natural populations of predators and parasitoids to artificially induced volatile emissions in maize plants (Zea mays L.). Agric For Entomol 3: 201-209.
14. von Merey G, Veyrat N, Mahuku G, Valdez RL, Turlings TCJ, et al. (2011) Dispensing synthetic green leaf volatiles in maize fields increases the release of sesquiterpenes by the plants, but has little effect on the attraction of pest and beneficial insects. Phytochemistry 72: 1838-1847.
15. von Merey GE, Veyrat N, de Lange E, Degen T, Mahuku G, et al. (2012) Minor effects of two elicitors of insect and pathogen resistance on volatile emissions and parasitism of Spodoptera frugiperda in Mexican maize fields. Biol Control 60: 7-15.
16. Heil M, (2004) Induction of two indirect defences benefits Lima bean (Phaseolus lunatus, Fabaceae) in nature. J Ecol 92: 527-536.
17. James DG, (2003) Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: Methyl salicylate and the green lacewing, Chrysopa nigricornis. J Chem Ecol 29: 1601-1609.
18. Poelman EH, Oduor AMO, Broekgaarden C, Hordijk CA, Jansen JJ, et al. (2009) Field parasitism rates of caterpillars on Brassica oleracea plants are reliably predicted by differential attraction of Cotesia parasitoids. Funct Ecol 23: 951-962.
19. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, et al. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434: 732-737.
20. Degenhardt J, Hiltpold I, Köllner TG, Frey M, Gierl A, et al. (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. P Natl Acad Sci USA 106: 13213-13218.
21. Gouinguené S, Degen T, Turlings TCJ, (2001) Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11: 9-16.
22. Degen T, Dillmann C, Marion-Poll F, Turlings TCJ, (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135: 1928-1938.
23. Kranz J, Schmutterer H, Koch W (1977) Diseases, Pests and Weeds of Tropical Crops. Berlin & Hamburg: Verlag Paul Parey.
24. Bottrell DG, Barbosa P, Gould F, (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annu Rev Entomol 43: 347-367.
25. Turlings TCJ, Ton J, (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr Opin Plant Biol 9: 421-427.
26. Fritzsche Hoballah ME, Turlings TCJ, (2001) Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evol Ecol Res 3: 553-565.
27. Hoballah ME, Degen T, Bergvinson D, Savidan A, Tamò C, et al. (2004) Occurrence and direct control potential of parasitoids and predators of the fall armyworm (Lepidoptera: Noctuidae) on maize in the subtropical lowlands of Mexico. Agric For Entomol 6: 83-88.
28. Wiseman BR, Davis FM, Campbell JE, (1980) Mechanical Infestation Device Used in Fall Armyworm Plant-Resistance Programs (Lepidoptera, Noctuidae). Fla Entomol 63: 425-432.
29. Carroll MJ, Schmelz EA, Teal PEA, (2008) The attraction of Spodoptera frugiperda neonates to cowpea seedlings is mediated by volatiles induced by conspecific herbivory and the elicitor inceptin. J Chem Ecol 34: 291-300.
30. Sparks AN, (1979) A review of the biology of the fall army worm. Fla Entomol 62: 82-87.
31. Bergvinson DJ, Hamilton RI, Arnason JT, (1995) Leaf profile of maize resistance factors to European corn borer, Ostrinia nubilalis. J Chem Ecol 21: 343-354.
32. Turlings TCJ, Davidson AC, Tamò C, (2004) A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol Entomol 29: 45-55.
33. Yang G, Wiseman BR, Espelie KE, (1993) Movement of Neonate Fall Armyworm (Lepidoptera: Noctuidae) Larvae on Resistant and Susceptible Genotypes of Corn. Environ Entomol 22: 547-553.
34. Paré PW, Tumlinson JH, (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114: 1161-1167.
35. Köllner TG, Schnee C, Gershenzon J, Degenhardt J, (2004) The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distribution. Phytochemistry 65: 1895-1902.
36. Gouinguené S (2000) Specificity and Variability of Induced Volatile Signalling in Maize Plants [Doctoral Thesis]. Neuchâtel: University of Neuchâtel. 156 p.
37. de Lange ES (2008) Suppression of maize indirect defenses by a specialist lepidopteran herbivore [Master thesis]. Utrecht: Utrecht University. 51 p.
38. Chown SL, Nicolson SW (2004) Insect Physiological Ecology: Mechanisms and Patterns: Oxford University Press. 254 p.
39. Yarro JG, (1985) Effect of host plant on moulting in the African armyworm Spodoptera exempta (Walk.) (Lepidoptera: Noctuidae) at constant temperature and humidity conditions. Insect Science and its Applications 6: 171-175.
40. Erb M, Balmer D, De Lange ES, Von Merey G, Planchamp C, et al. (2011) Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots. Plant Cell Environ 34: 1088-1103.
41. Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH, Teal PEA, (2009) Phytohormone-based activity mapping of insect herbivore-produced elicitors. P Natl Acad Sci USA 106: 653-657.
42. Benrey B, Denno RF, (1997) The slow-growth-high-mortality hypothesis: a test using the cabbage butterfly. Ecology 78: 987-999.
43. Karimzadeh J, Wright DJ, (2008) Bottom-up cascading effects in a tritrophic system: interactions between plant quality and host-parasitoid immune responses. Ecol Entomol 33: 45-52.
44. Turlings TCJ, Benrey B, (1998) Effects of plant metabolites on the behavior and development of parasitic wasps. Ecoscience 5: 321-333.
45. Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT, (2008) Shared signals - 'alarm calls' from plants increase apparency to herbivores and their enemies in nature. Ecol Lett 11: 24-34.
46. James DG, Price TS, (2004) Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J Chem Ecol 30: 1613-1628.
47. De Boer JG, Dicke M, (2004) The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J Chem Ecol 30: 255-271.
48. Gouinguené S, Pickett JA, Wadhams LJ, Birkett MA, Turlings TCJ, (2005) Antennal electrophysiological responses of three parasitic wasps to caterpillar-induced volatiles from maize (Zea mays mays), cotton (Gossypium herbaceum), and cowpea (Vigna unguiculata). J Chem Ecol 31: 1023-1038.
49. D'Alessandro M, Turlings TCJ, (2005) In-situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chem Senses 30: 739-753.
50. D'Alessandro M, Brunner V, von Mérey G, Turlings TCJ, (2009) Strong Attraction of the Parasitoid Cotesia marginiventris Towards Minor Volatile Compounds of Maize. J Chem Ecol 35: 999-1008.
51. Hoballah ME, Turlings TCJ, (2005) The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J Chem Ecol 31: 2003-2018.
52. D'Alessandro M, Held M, Triponez Y, Turlings TCJ, (2006) The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J Chem Ecol 32: 2733-2748.
53. Tamò C, Ricard I, Held M, Davison AC, Turlings TCJ, (2006) A comparison of naive and conditioned responses of three generalist endoparasitoids of lepidopteran larvae to host-induced plant odours. Anim Biol 56: 205-220.
54. Fritzsche Hoballah ME, Tamò C, Turlings TCJ, (2002) Differential attractiveness of induced odors emitted by eight maize varieties for the parasitoid Cotesia marginiventris: is quality or quantity Important? J Chem Ecol 28: 951-968.
55. Hunter MD, (2002) A breath of fresh air: beyond laboratory studies of plant volatile-natural enemy interactions. Agric For Entomol 4: 81-86.
56. Degenhardt J, Gershenzon J, Baldwin IT, Kessler A, (2003) Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr Opin Biotechnol 14: 169-176.
57. Furlong MJ, Zalucki MP, (2010) Exploiting predators for pest management: the need for sound ecological assessment. Entomol Exp Appl 135: 225-236.