Skip to main content
Log in

Does Singular and Stacked Corn Affect Choice Behavior for Oviposition and Feed in Spodoptera frugiperda (Lepidoptera: Noctuidae)?

  • Pest Management
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

Little is known about the effects of genetically modified corn plants on the foraging of Spodoptera frugiperda (J.E. Smith). Therefore, this study examines whether singular herbicide-tolerant and insect-resistant plants and their stacked events interfere with food preference and oviposition of S. frugiperda. Two non-Bt corn hybrids and three Bt-hybrids, some of them with glyphosate tolerance (GT), were evaluated. Food preference of larvae and biological parameters were assessed. Oviposition preference bioassays involved choice and no choice condition in plants uninfested and previously infested by larvae in a greenhouse and in the field. The results indicate that there is no relationship between preference of larvae and adult moths. Adult females selected preferentially transgenic hybrids, while larvae selected non-Bt hybrid. Fall armyworm larvae avoid Bt-toxin-expressing leaf tissues, survived only on the non-Bt leaf tissues, and showed minor differences in other life-history traits reared on GT and non-transgenic corn leaf tissues. Female moths showed preference for transgenic plants to lay eggs, but with variable output between previously infested and uninfested plants with larvae. The fact that moths preferred Ag 3700RR2 and non-Bt hybrids for oviposition supports the refuge’s strategy aiming at producing susceptible individuals. The use of this hybrid must be integrated with a program of control. The results showed also the importance of correct hybrid selection as part of insect resistance management to Bt-plants. The implications of these findings for understanding the impacts of plant-mediated cues on pest behavior in transgenic crop systems are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig 1
Fig 2
Fig 3
Fig 4
Fig 5

Similar content being viewed by others

References

  • Bellota E, Da ́vila-Flores A, Bernal JS (2017) A bird in the hand versus two in the bush? The specialist leaf-hopper Dalbulus maidis (Hemiptera: Cicadellidae) does not discriminate againstsub-optimal hostplants (Zea spp.). Neotrop Entomol 47:171–180

    Article  PubMed  Google Scholar 

  • Bestete LR, Torres JB, Silva RBB, Silva-Torres CSA (2016) Water stress and kaolin spray affect herbivorous insects’ success on cotton. Arth Plant Int 10:445–453

    Article  Google Scholar 

  • Bestete LR, Torres JB, Silva RBB, Silva-Torres CSA, Bastos CS (2017) Development of cotton pests exhibiting different feeding strategy on water-stressed and kaolin-treated cotton plants. J Pest Sci 90:39–150

    Article  Google Scholar 

  • Carriere Y (1992) Host plant exploitation within a population of a generalist herbivore, Choristoneura rosaceana. Entomol Exp Appl 65:11–19

    Article  Google Scholar 

  • Carroll MJ, Schmelz EA, Meagher RL, Teal PEA (2006) Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. J Chem Ecol 32:1911–1924

    Article  CAS  PubMed  Google Scholar 

  • Chapman JW, Williams T, Martínez AM, Cisneros J, Caballero P, Cave RD, Goulson D (2000) Does cannibalism in Spodoptera frugiperda (Lepidoptera: Noctuidae) reduce the risk of predation? Behav Ecol Sociobiol 48:321–327

    Article  Google Scholar 

  • Crawley MJ (2013) The R book, 2nd edn. JohnWiley & Sons, Chichester

    Google Scholar 

  • Cruz I, Turpin FT (1982) Efeito da Spodoptera frugiperda em diferentes estágios de crescimento da cultura do milho. Pesq Agropec Bras 17:355–359

    Google Scholar 

  • De la Rosa-Cancino W, Rojas JC, Cruz-Lopez L, Castillo A (2016) Attraction, feeding preference, and performance of Spodoptera frugiperda larvae (Lepidoptera: Noctuidae) reared on two varieties of maize. Environ Entomol 45:384–389

    Article  Google Scholar 

  • De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced noctural plant volatiles repel conspecific females. Nature 410:577–580

    Article  CAS  PubMed  Google Scholar 

  • Dean JM, De Moraes CM (2006) Effects of genetic modification on herbivore-induced volatiles from maize. J Chem Ecol 32:713–724

    Article  CAS  PubMed  Google Scholar 

  • Doak P (2000) Population consequences of restricted dispersal for an insect herbivore in a subdivided habitat. Ecology 81:1828–1841

    Article  Google Scholar 

  • Fatouros NE, Lucas-Barbosa D, Weldegergis BT, Pashalidou FG, van Loon JJ, 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

    Article  CAS  Google Scholar 

  • Head GP, Carroll MW, Evans SP, Rule DW, Willse AR, Clark TL, Storer NP, Flannagan RD, Samuel LW, Meinke LJ (2017) Evaluation of SmartStax and SmartStax PRO maize against western corn rootworm and northern corn rootworm: efficacy and resistance management. Pest Manag Sci 73:1883–1899

    Article  CAS  PubMed  Google Scholar 

  • Hellmich R, Higgins L, Witkowski J, Campbell J, Lewis L (1999) Oviposition by European corn borer (Lepidoptera: Crambidae) in response to various transgenic corn events. J Econ Entomol 92:1014–1020

    Article  Google Scholar 

  • Hilker M, Fatouros NE (2015) Plant responses to insect egg deposition. Annu Rev Entomol 60:493–515

    Article  CAS  PubMed  Google Scholar 

  • ISAAA (2018) Global status of commercialized biotech/GM crops: 2018. https://www.isaaa.org/resources/publications/briefs/ accessed 10 Fev 2019

  • Lei Z, Liu T, Greenberg S (2009) Feeding, oviposition and survival of Liriomyza trifolii (Diptera: Agromyzidae) on Bt and non-Bt cottons. Bull Entomol Res 99:3

    Article  Google Scholar 

  • Musser RA, Hum-Musser S, Eichenseer H, Peiffer M, Ervin G, Murphy B, Felton GW (2002) Caterpillar saliva beats plant defences: a new weapon emerges in the evolutionary arms race between plants and herbivores. Nature 416:599–600

    Article  CAS  PubMed  Google Scholar 

  • Mustapha FAJ, Myron PZ (2003) Relationship between oviposition preference and offspring performance in Australian Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) Aust. J Entomol 42:343–348

    Google Scholar 

  • Nylin S, Janz N, Wedell N (1996) Oviposition plant preference and offspring performance in the comma butterfly: correlations and conflicts. Entomol Exp Appl 80:141–144

    Article  Google Scholar 

  • Penaflor MF, Erb M, Robert CA, Miranda LA, Werneburg AG, Alda Dossi FC, Turlings TCJ, Bento JM (2011) Oviposition by a moth suppresses constitutiveand herbivore-induced plant volatiles in maize. Planta 234:207–215

    Article  CAS  PubMed  Google Scholar 

  • Pitre HN, Mulrooney JE, Hogg DB (1983) Fall armyworm (Lepidoptera: Noctuidae) oviposition: crop preferences and egg distribution on plants. J Econ Entomol 76:463–466

    Article  Google Scholar 

  • R Core Team (2014) A language and environment for statistical computing. R Foundation for statistical computing. Vienna. New Delhi, India, p 977

    Google Scholar 

  • Refsnider JM, Janzen FJ (2010) Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Annu Rev Ecol Syst 41:39–57

    Article  Google Scholar 

  • Richardson ML, Mitchell RF, Reagel PF, Hanks LM (2009) Causes and consequences of cannibalism in non carnivorous insects. Annu Rev Entomol 55:39–53

    Article  CAS  Google Scholar 

  • Robert CAM, Erb M, Hiltpold I, Hibbard BE, Gaillard MDP, Bilat J, Degenhardt J, Cambet-Petit-Jean X, Turlings TC, Zwahlen C (2013) Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field. Plant Biotechnol J 11:628–639

    Article  CAS  PubMed  Google Scholar 

  • Rojas JC, Kolomiets MV, Bernal JS (2018) Nonsensical choices? Fall armyworm moths choose seemingly best or worst hosts for their larvae, but neonate larvae make their own choices. PLoS One 13:e0197628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology. Oxford University Press, New York

    Google Scholar 

  • Schuler TH, Potting RP, Denholm I, Poppy GM (1999) Parasitoid behaviour and Bt plants. Nature 400:825–829

    Article  CAS  PubMed  Google Scholar 

  • Signoretti AGC, Peñaflor MFGV, Bento JMS (2012) Fall armyworm, Spodoptera frugiperda (J.E. smith) (Lepidoptera: Noctuidae), female moths respond to herbivore-induced corn volatiles. Neotrop Entomol 41:22–26

    Article  CAS  PubMed  Google Scholar 

  • Singer MS, Stireman JO (2001) How foraging tactics determine host-plant use by a polyphagous caterpillar. Oecologia 129:98–105

    Article  CAS  PubMed  Google Scholar 

  • Singer MS, Stireman JO (2003) Does anti-parasitoid defense explain host-plant selection by a polyphagous caterpillar? Oikos 100:554–562

    Article  Google Scholar 

  • Singer MS, Bernays EA, Carriere Y (2002) The interplay between nutrient balancing and toxin dilution in foraging by a generalist insect herbivore. Anim Behav 64:629–643

    Article  Google Scholar 

  • Sparks AN (1979) A review of the biology of the fall armyworm. Fla Entomol 62:82–86

    Article  Google Scholar 

  • Storer NP, Kubiszak ME, Ed King J, Thompson GD, Santos AC (2012) Status of resistance to Bt maize in Spodoptera frugiperda: lessons from Puerto Rico. J Invertebr Pathol 110:294–300

    Article  PubMed  Google Scholar 

  • Szczepaniec A, Widney SE, Bernal JS, Eubanks MD (2013) Higher expression of induced defenses in teosintes (Zea spp.) is correlated with greater resistance to fall armyworm, Spodoptera frugiperda. Entomol Exp Appl 146:242–251

    Article  Google Scholar 

  • Téllez-Rodríguez P, Raymond B, Morán-Bertot I, Rodríguez-Cabrera L, Wright DJ, Borroto CG, Ayra-Pardo C (2014) Strong oviposition preference for Bt over non-Bt maize in Spodoptera frugiperda and its implications for the evolution of resistance. BMC Biol 12:48

    Article  PubMed  PubMed Central  Google Scholar 

  • Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14

    Article  Google Scholar 

  • Torres JB, Ruberson JR (2006) Spatial and temporal dynamics of oviposition behavior of bollworm and three of its predators in Bt and non-Bt cotton fields. Entomol Exp Appl 120:11–22

    Article  Google Scholar 

  • Turlings TCJ, Jeanbourquin PM, Held M, Degen T (2005) Evaluating the induced-odour emission of a Bt maize and its attractiveness to parasitic wasps. Transgenic Res 14:807–816

    Article  CAS  PubMed  Google Scholar 

  • Udayagiri S, Mason CE (1995) Host plant constituents as oviposition stimulants for a generalist herbivore: European corn borer. Entomol Exp Appl 76:59–65

    Article  Google Scholar 

  • Valicente FH, Barreto MR (2003) Bacillus thuringiensis survey in Brazil: geographical distribution and insecticidal activity against Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). Neotrop Entomol 32:639–644

    Article  Google Scholar 

  • Yang G, Wiseman BR, Isenhour DJ, Espelie KE (1993) Chemical and ultrastructural analysis of corn cuticular lipids and their effect on feeding by fall armyworm larvae. J Chem Ecol 19:2055–2074

    Article  CAS  PubMed  Google Scholar 

  • Zalucki MP, Clarke AR, Malcolm SB (2002) Ecology and behavior of first instar larval Lepidoptera. Annu Rev Entomol 47:361–393

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Programa de Pós-Graduação em Agronomia/Fitotecnia, for the scientific support to the student and thank Embrapa Milho e Sorgo, for the structure provided for the experiment.

Author Contribution Statement

PT Nascimento planed, designed and executed experimental work, MAM Fadini conducted data analyses, PT Nascimento wrote the manuscript. FH Valicente, MAM Fadini, CSF Souza and RG Von Pinho reviewed the manuscript.

Funding

The study was financially supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. H. Valicente.

Additional information

Edited by Jorge B Torres – UFRPE

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nascimento, P.T., Von Pinho, R.G., Fadini, M.A.M. et al. Does Singular and Stacked Corn Affect Choice Behavior for Oviposition and Feed in Spodoptera frugiperda (Lepidoptera: Noctuidae)?. Neotrop Entomol 49, 302–310 (2020). https://doi.org/10.1007/s13744-019-00750-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-019-00750-0

Keywords

Navigation