Attraction of the parasitoid Cotesia marginiventris to host (Spodoptera frugiperda) frass is affected by transgenic maize

Ecotoxicology

Volumn 19, Issue 7, 2010, Pages 1183-1192

  Desneux, Nicolas ^a   Ramírez Romero, Ricardo ^b   Bokonon Ganta, Aimé H ^c   Bernal, Julio S ^d  

^a CEMAGREF   (France)

^b UNIVERSITY OF GUADALAJARA   (Mexico)

^c Service de Protection des Végétaux   (Benin)

^d NONE

Author keywords

Bacillus thuringiensis; Biological control; Bt; Kairomones; Non target effects; Spodoptera frugiperda; Sublethal effects

Indexed keywords

BACILLUS THURINGIENSIS TOXIN; TETRACYCLINE;

ANTIBIOTICS; BIOLOGICAL CONTROL; KAIROMONE; MAIZE; PARASITOID; SEEDLING; SUBLETHAL EFFECT;

ANIMAL EXPERIMENT; ARTICLE; BACILLUS THURINGIENSIS; BIOLOGICAL PEST CONTROL; CONTROLLED STUDY; COTESIA MARGINIVENTRIS; CULTIVAR; FEMALE; FORAGING BEHAVIOR; HOST PARASITE INTERACTION; LEPIDOPTERA; MAIZE; NONHUMAN; ODOR; PARASITOID; PRIORITY JOURNAL; SEEDLING; TRANSGENIC CROP;

ANIMALS; BACILLUS THURINGIENSIS; ENDOTOXINS; FEMALE; ODORS; PEST CONTROL, BIOLOGICAL; PHEROMONES; PLANTS, GENETICALLY MODIFIED; SEEDLING; SPODOPTERA; WASPS; ZEA MAYS;

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); COTESIA MARGINIVENTRIS; SPODOPTERA FRUGIPERDA; ZEA MAYS;

EID: 78149469476     PISSN: 09639292     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10646-010-0502-3     Document Type: Article

References (73)

1. AgBios (2009) Database product description: MON810. The AgBios Company. http://www.agbios.com/dbase.php?action=Submit&evidcode=MON810. Accessed 12 March 2010
2. NG Agelopoulos M Dicke MA Posthumus 1995 Role of volatile infochemicals emitted by feces of larvae in host-searching behavior of parasitoid Cotesia rubecula (Hymenoptera: Braconidae): a behavioral and chemical study J Chem Ecol 21 1789 1811 1:CAS:528:DyaK2MXhtVShs7bO 10.1007/BF02033677
3. DA Andow GL Lovei S Arpaia 2006 Ecological risk assessment for Bt crops Nat Biotechnol 24 749 751 1:CAS:528:DC%2BD28XmvFagtbw%3D 10.1038/nbt0706-749 (Pubitemid 44086606)
4. E Aranda J Sanchez M Peferoen L Guereca A Bravo 1996 Interactions of Bacillus thuringiensis crystal proteins with the midgut epithelial cells of Spodoptera frugiperda (Lepidoptera: Noctuidae) J Invertebr Pathol 68 203 212 1:CAS:528:DyaK28XnsVals78%3D 10.1006/jipa.1996.0087 (Pubitemid 126321239)
5. TR Ashley 1986 Geographical distribution and parasitization levels of parasitoids of the fall armyworm, Spodoptera frugiperda Fla Entomol 69 516 524 10.2307/3495384
6. J Auger C Lecomte E Thibout 1990 Origin of kairomones in the leek moth (Acrolepiopsis assectella, Lep.) frass. Possible pathway from methylthio to propylthio compounds J Chem Ecol 16 1743 1750 1:CAS:528:DyaK3cXltFaksb4%3D 10.1007/BF01020491
7. Bernal JS (2010) Genetically modified crops and biological control with egg parasitoids. In: Consoli FL, Parra JRP, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma (Progress in biological control). Springer, Amsterdam (in press)
8. JS Bernal M Sétamou 2003 Fortuitous antixenosis in transgenic sugarcane: antibiosis-expressing cultivar deters oviposition by herbivore pests Environ Entomol 32 886 894 10.1603/0046-225X-32.4.886
9. Bernal JS, Prasifka J, Sétamou M, Heinz KM (2004) Transgenic insecticidal cultivars in integrated pest management: challenges and opportunities. In: Koul O, Dhaliwal GS, Cuperus G (eds) Integrated pest management: potential, constraints and challenges. CABI Publishing, Wallingford, pp 123-145
10. AH Bokonon-Ganta JS Bernal PV Pietrantonio M Sétamou 2003 Survivorship and development of fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), on conventional and transgenic maize cultivars expressing Bacillus thuringiensis Cry9C and Cry1A(b) endotoxins Int J Pest Manag 49 169 175 1:CAS:528:DC%2BD3sXktVGktLw%3D 10.1080/0967087031000085024 (Pubitemid 36720441)
11. NA Broderick KF Raffa J Handelsman 2006 Midgut bacteria required for Bacillus thuringiensis insecticidal activity Proc Natl Acad Sci USA 103 15196 15199 1:CAS:528:DC%2BD28XhtFamurrO 10.1073/pnas.0604865103 (Pubitemid 44583187)
12. NA Broderick CJ Robinson MD McMahon J Holt J Handelsman KF Raffa 2009 Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera BMC Biol 7 11 10.1186/1741-7007-7-11
13. P Chiu-Alvarado JF Barrera JC Rojas 2009 Attraction of Prorops nasuta (Hymenoptera: Bethylidae) a parasitoid of the coffee berry borer (Coleoptera: Curculionidae), to host-associated olfactory cues Ann Entomol Soc Am 102 166 171 10.1603/008.102.0119
14. J Chuche A Xuereb D Thiery 2006 Attraction of Dibrachys cavus (Hymenoptera: Pteromalidae) to its host frass volatiles J Chem Ecol 32 2721 2731 1:CAS:528:DC%2BD28Xht1Ogs7nN 10.1007/s10886-006-9195-8 (Pubitemid 44912434)
15. IZ de Polanía HAA Maldonado RM Cruz JLD Sánchez 2009 Spodoptera frugiperda: respuesta de distintas poblaciones a la toxina Cry1Ab Rev Colomb Entomol 35 34 41
16. JM Dean CM De Moraes 2006 Effects of genetic modification on herbivore-induced volatiles from maize J Chem Ecol 32 713 724 1:CAS:528:DC%2BD28XkvVOhtr8%3D 10.1007/s10886-006-9040-0 (Pubitemid 43804597)
17. N Desneux MH Pham-Delègue L Kaiser 2004 Effects of sublethal and lethal doses of lambda-cyhalothrin on oviposition experience and host searching behaviour of a parasitic wasp, Aphidius ervi Pest Manag Sci 60 381 389 1:CAS:528:DC%2BD2cXivVSktrw%3D 10.1002/ps.822 (Pubitemid 38436300)
18. N Desneux A Decourtye JM Delpuech 2007 The sublethal effects of pesticides on beneficial arthropods Annu Rev Entomol 52 81 106 1:CAS:528:DC%2BD2sXhtFWnurw%3D 10.1146/annurev.ento.52.110405.091440 (Pubitemid 46133563)
19. RJ Dillon VM Dillon 2004 The gut bacteria of insects: non-pathogenic interactions Annu Rev Entomol 49 71 92 1:CAS:528:DC%2BD2cXhtFKrsrk%3D 10.1146/annurev.ento.49.061802.123416 (Pubitemid 38192417)
20. Dudai Y (1989) The neurobiology of memory. Oxford University Press, New York
21. ME Favret AA Yousten 1989 Thuricin: the bacteriocin produced by Bacillus thuringiensis J Invertebr Pathol 53 206 216 1:CAS:528:DyaL1MXhvV2jsLY%3D 10.1016/0022-2011(89)90009-8 (Pubitemid 19087303)
22. RS Hakim K Baldwin G Smagghe 2010 Regulation of midgut growth, development, and metamorphosis Annu Rev Entomol 55 593 608 1:CAS:528: DC%2BC3cXptVSgtw%3D%3D 10.1146/annurev-ento-112408-085450
23. A Hilbeck JEU Schmidt 2006 Another view on Bt proteins-how specific are they and what else might they do? Biopestic Int 2 1 50
24. C Inayatullah 1983 Host selection by Apanteles flavipes (Cameron) (Hymenoptera: Braconidae): influence of host and host plant J Econ Entomol 76 1086 1087
25. James C (2004) Global status of commercialised biotech/GMcrops: 2004. ISAAA Briefs, No. 32. International Service for the Acquisition of Agri-Biotech Applications, Ithaca, NY
26. A Krieg 1970 Thuricin, a bacteriocin produced by Bacillus thuringiensis J Invertebr Pathol 15 291 10.1016/0022-2011(70)90251-X
27. WH Loke TR Ashley 1984 Behavioral and biological response of Cotesia marginiventris to kairomones of the fall armyworm, Spodoptera frugiperda J Chem Ecol 10 521 529 1:CAS:528:DyaL2cXhs12qsLw%3D 10.1007/BF00988097
28. GL Lovei DA Andow S Arpaia 2009 Transgenic insecticidal crops and natural enemies: a detailed review of laboratory studies Environ Entomol 38 293 306 10.1603/022.038.0201
29. B Lumbierres R Albajes X Pons 2004 Transgenic Bt maize and Rhopalosiphum padi (Hom., Aphididae) performance Ecol Entomol 29 309 317 10.1111/j.0307-6946. 2004.00597.x (Pubitemid 38751612)
30. JG Lundgren AJ Gassmann J Bernal JJ Duan J Ruberson 2009 Ecological compatibility of GM crops and biological control Crop Prot 28 1017 1030 10.1016/j.cropro.2009.06.001
31. Marsh PM, Carlson RW (1979) Superfamily Ichneumonoidea. In: Krombein KV, Hurd PD Jr, Smith DR, Burks BD (eds) Catalog of Hymenoptera of America north of Mexico. Smithsonian Institution Press, Washington, DC, pp 143-741
32. L Mattiacci M Dicke 1995 The parasitoid Cotesia glomerata (Hymenoptera: Braconidae) discriminates between first and fifth larval instars of its host Pieris brassicae, on the basis of contact cues from frass, silk, and herbivore-damaged leaf tissue J Insect Behav 8 485 498 10.1007/BF01995321
33. R Meyhöfer J Casas S Dorn 1994 Host location by a parasitoid using leafminer vibrations-characterizing the vibrational signals produced by the leafmining host Physiol Entomol 19 349 359 10.1111/j.1365-3032.1994.tb01062.x
34. R Monnerat E Martins P Queiroz, et al. 2006 Genetic variability of Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) populations from Latin America is associated with variations in susceptibility to Bacillus thuringiensis Cry toxins Appl Environ Microbiol 72 7029 7035 1:CAS:528:DC%2BD28Xht1Gksr7O 10.1128/AEM.01454-06 (Pubitemid 44748415)
35. LG Monteith 1963 Habituation and associative learning in Drino bohemica Mesn. (Diptera: Tachinidae) Can Entomol 95 418 426 10.4039/Ent95418-4
36. AJ Ngi-Song WA Overholt 1997 Host location and acceptance by Cotesia flavipes Cameron and C. sesamiae (Cameron) (Hymenoptera: Braconidae), parasitoids of African gramineous stemborers: role of frass and other host cues Biol Control 9 136 142 10.1006/bcon.1997.0524 (Pubitemid 27307490)
37. M O'Callaghan TR Glare EPJ Burgess LA Malone 2005 Effects of plants genetically modified for insect resistance on nontarget organisms Annu Rev Entomol 50 271 292 10.1146/annurev.ento.50.071803.130352
38. AA Olesinski WJ Lucas E Galun S Wolf 1995 Pleiotropic effects of tobacco-mosaic-virus movement protein on carbon metabolism in transgenic tobacco plants Planta 197 118 126 1:CAS:528:DyaK2MXnvVKrtrY%3D 10.1007/BF00239947
39. IR Pendleton 1969 Ecological significance of antibiotics of some varieties of Bacillus thuringiensis J Invertebr Pathol 13 235 240 1:STN:280:DyaF1M7lslehtg%3D%3D 10.1016/0022-2011(69)90214-6
40. RPJ Potting LEM Vet M Dicke 1995 Host microhabitat location by stem-borers parasitoids Cotesia flavipes: the role of herbivore volatiles and locally and sytemically induced plant volatiles J Chem Ecol 21 525 539 1:CAS:528:DyaK2MXmt1Sgu7c%3D 10.1007/BF02033699
41. Ramírez-Romero R (2004) Side effects of the Bt endotoxin Cry1Ab and of insecticides on biological and behavioural traits of the honey bee Apis mellifera and the parasitoid Cotesia marginiventris. PhD dissertation, University of Paris XIII, France
42. R Ramírez-Romero J Chaufaux MH Pham-Delègue 2005 Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach Apidologie 36 601 611 10.1051/apido:2005039 (Pubitemid 41826534)
43. R Ramírez-Romero JS Bernal J Chaufaux L Kaiser 2007 Impact assessment of Bt-maize on a moth parasitoid, Cotesia marginiventris (Hymenoptera: Braconidae), via host exposure to purified Cry1Ab protein or Bt-plants Crop Prot 26 953 962 10.1016/j.cropro.2006.09.001 (Pubitemid 46719525)
44. R Ramírez-Romero N Desneux A Decourtye A Chaffiol MH Pham-Delègue 2008 Does Cry1Ab protein affect learning performances of the honey bee Apis mellifera L? Ecotoxicol Environ Saf 70 327 333 10.1016/j.ecoenv.2007.12.002
45. J Romeis M Meissle F Bigler 2006 Transgenic crops expressing Bacillus thuringiensis toxins and biological control Nat Biotechnol 24 63 71 1:CAS:528:DC%2BD28XisVGktg%3D%3D 10.1038/nbt1180 (Pubitemid 43083167)
46. USR Rose HT Alborn G Makranczy WJ Lewis JH Tumlinson 1997 Host recognition by the specialist endoparasitoid Microplitis croceipes J Insect Behav 10 313 330 10.1007/BF02765600
47. JR Ruberson GA Herzog WR Lambert WJ Lewis 1994 Management of beet armyworm (Lepidoptera: Noctuidae) in cotton: role of natural enemies Fla Entomol 77 440 453 10.2307/3495698
48. CJ Sanders JK Pell GM Poppy A Raybould M Garcia-Alonso TH Schuler 2007 Host-plant mediated effects of transgenic maize on the insect parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae) Biol Control 40 362 369 10.1016/j.biocontrol.2006.12.010 (Pubitemid 46206133)
49. JC Sandoz D Laloi JF Odoux MH Pham-Delègue 2000 Olfactory information transfer in the honeybee: compared efficiency of classical conditioning and early exposure Anim Behav 59 1025 1034 10.1006/anbe.2000.1395 (Pubitemid 30656577)
50. TH Schuler RPJ Potting I Denholm GM Poppy 1999 Parasitoid behavior and Bt plants Nature 400 825 826 1:CAS:528:DyaK1MXlslGgtb4%3D 10.1038/23605 (Pubitemid 29406709)
51. TH Schuler RPJ Potting I Denholm SJ Clark AJ Clark CN Stewart GM Poppy 2003 Tritrophic choice experiments with Bt plants, the diamondback moth (Plutella xylostella) and the parasitoid Cotesia plutellae Transgenic Res 12 351 361 1:CAS:528:DC%2BD3sXivFymsr4%3D 10.1023/A:1023342027192 (Pubitemid 36573223)
52. M Sétamou JS Bernal JC Legaspi TE Mirkov 2002 Parasitism and location of sugarcane borer hosts by Cotesia flavipes (Cameron) (Hymenoptera: Braconidae) on transgenic and conventional sugarcane Environ Entomol 31 1219 1225 10.1603/0046-225X-31.6.1219
53. AN Sparks 1979 A review of the biology of the fall armyworm Fla Entomol 62 82 87 10.2307/3494083
54. E Thibout JF Guillot J Auger 1993 Microorganisms are involved in the production of volatile kairomones affecting the host seeking behaviour of Diadromus pulchellus, a parasitoid of Acrolepiopsis assectella Physiol Entomol 18 176 182 1:CAS:528:DyaK3sXmt1aitrk%3D 10.1111/j.1365-3032.1993.tb00465.x
55. E Thibout JF Guillot S Ferary P Limouzin J Auger 1995 Origin and identification of bacteria which produce kairomones in the frass of Acrolepiopsis assectella (Lep., Hyponomeutoidea) Experientia 51 1073 1075 1:CAS:528:DyaK2MXpvVGltLc%3D 10.1007/BF01946919
56. BW Tomov S Bernal SB Vinson 2003 Impacts of transgenic sugarcane expressing GNA on parasitism of Mexican rice borer by Parallorhogas pyralophagus (Marsh) (Hymenoptera: Braconidae) Environ Entomol 32 866 872 10.1603/0046-225X-32.4.866
57. TCJ Turlings JH Tumlinson WJ Lewis 1990 Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps Science 250 1251 1253 1:CAS:528:DyaK3MXpvVKktA%3D%3D 10.1126/science.250.4985.1251
58. TCJ Turlings PJ McCall HT Alborn JH Tumlinson 1993 An elicitor in caterpillar oral secretions that induces maize seedlings to emit chemical signals attractive to parasitic wasps J Chem Ecol 19 411 425 1:CAS:528:DyaK3sXisFWku7w%3D 10.1007/BF00994314
59. TCJ Turlings PM Jeanbourquin M Held T Degen 2005 Evaluating the induced-odour emission of a Bt maize and its attractiveness to parasitic wasps Transgenic Res 14 807 816 1:CAS:528:DC%2BD2MXht1Glt7zK 10.1007/s11248-005-0008-6 (Pubitemid 41706046)
60. B Überlacker B Klinge W Werr 1996 Ectopic expression of the maize homeobox genes ZmHox1a or ZmHox1b causes pleiotropic alterations in the vegetative and floral development of transgenic tobacco Plant Cell 8 349 362 10.1105/tpc.8.3.349
61. MB van Leerdam JW Smith Jr TW Fuchs 1985 Frass-mediated host-finding behavior of Cotesia flavipes, a braconid parasite of Diatraea saccharalis (Lepidoptera: Pyralidae) Ann Entomol Soc Am 78 647 650
62. LEM Vet M Dicke 1992 Ecology of infochemical use by natural enemies in a tritrophic context Annu Rev Entomol 37 141 172 10.1146/annurev.en.37.010192. 001041
63. LEM Vet JC van Lenteren M Heymans E Meelis 1983 An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects Physiol Entomol 8 97 106 10.1111/j.1365-3032.1983.tb00338.x
64. Vinson SB (1984) How parasitoids locate their hosts: a case of insect espionage. In: Lewis T (ed) Insect communication. Academic Press, London, pp 325-348
65. SB Vinson 1991 Chemical signals used by parasitoids Redia 74 15 42
66. EG Virla A Álvarez F Loto LM Pera M Baigorí 2008 Fall armyworm strains (Lepidoptera: Noctuidae) in Argentina, their associate host plants and response to different mortality factors in laboratory Fla Entomol 91 63 69 1:CAS:528:DC%2BD1cXltFCqsL0%3D 10.1653/0015-4040(2008)091[0063:FASLNI]2.0. CO;2 (Pubitemid 351519908)
67. LE Visotto MGA Oliveira RNC Guedes AOB Ribon POV Good-God 2009 Contribution of gut bacteria to digestion and development of the velvetbean caterpillar, Anticarsia gemmatalis J Insect Physiol 55 185 191 1:CAS:528:DC%2BD1MXitVCqsrc%3D 10.1016/j.jinsphys.2008.10.017
68. E Vojtech M Meissle GM Poppy 2005 Effects of Bt maize on the herbivore Spodoptera littoralis (Lepidoptera: Noctuidae) and the parasitoid Cotesta marginiventris (Hymenoptera: Braconidae) Transgenic Res 14 133 144 1:CAS:528:DC%2BD2MXktFGhtb0%3D 10.1007/s11248-005-2736-z (Pubitemid 40747893)
69. GP Walker PJ Cameron FM MacDonald VV Madhusudhan AR Wallace 2007 Impacts of Bacillus thuringiensis toxins on parasitoids (Hymenoptera: Braconidae) of Spodoptera litura and Helicoverpa armigera (Lepidoptera: Noctuidae) Biol Control 40 142 151 1:CAS:528:DC%2BD28Xhtlalt77F 10.1016/j.biocontrol.2006.09.008 (Pubitemid 44880816)
70. YQ Wang XB Pan XW Cui SM Pan 1998 Research on the physiological traits of Bt transgenic cotton R93-4 China Cottons 25 14 16 1:CAS:528:DyaK1cXlvFGntLs%3D
71. MR Weiss 2006 Defecation behavior and ecology of insects Annu Rev Entomol 51 635 661 1:CAS:528:DC%2BD28XptlClsA%3D%3D 10.1146/annurev.ento.49.061802. 123212 (Pubitemid 43107837)
72. TG Yudina LI Burtseva 1997 Activity of delta-endotoxins of four Bacillus thuringiensis subspecies against prokaryotes Microbiology 66 17 22 1:CAS:528:DyaK2sXhtFCltLo%3D
73. TG Yudina ES Milko NS Egorov 1996 Sensitivity of Micrococcus luteus dissociation variants to delta-endotoxins of Bacillus thuringiensis Microbiology 65 321 325