Abstract
This study sought to provide relevant information for developing effective programs to manage Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) resistance to insecticides by quantifying and describing the interactions between cotton Bt and Podisus nigrispinus (Dallas) (Heteroptera; Pentatomidae) in the management of lambda-cyhalothrin resistance in S. frugiperda fed Bt cotton leaves expressing Cry1Ac (Bollgard, Monsanto, St Louis, MO, USA). These effects were assayed by studying functional responses. Third instar S. frugiperda larvae were used for the following treatments: strains resistant (1) or susceptible (2) to lambda-cyhalothrin fed Bollgard cotton leaves and strains resistant (3) or susceptible (4) to lambda-cyhalothrin fed non-Bt cotton leaves. The predatory behavior of P. nigrispinus females was best represented by a sigmoid curve. The type of P. nigrisinus functional response was not affected by the cotton cultivar or S. frugiperda strain used in the trials. P. nigrispinus females invested a greater amount of handling time (T h) in S. frugiperda larvae that were suseptible to insecticides and fed non-Bt cotton (T h = 1.72 h) compared to those from the insecticide-resistant strain fed with Bt cotton (T h = 1.23 h) or even compared to those that were lambda-cyhalothrin resistant and fed Bt (T h = 1.17 h) or non-Bt cotton (T h = 1.17 h). The results in the present study can be applied in the development of management programs targeting S. frugiperda resistance to pyrethroid lambda-cyhalothrin. The integration of Bt cotton concurrent with biological control by the Asopinae P. nigrispinus is important for successfully managing S. frugiperda resistance to lambda-cyhalothrin.
Similar content being viewed by others
References
Adamczyk Jr JJ, Greenberg S, Armstrong S Mullins WJ, Braxton LB, Lassiter RB, Siebert MW (2008) Evaluation of Bollgard II and WideStrike Technologies against beet and fall armyworms. In: Proceedings, Beltwide Cotton Conferences. National Cotton Council, Memphis, TN
Barros R (2012) Evaluation of Bt-cotton as strategy tool for the control of cotton plant-insects under field conditions. Cientifica 40:117–137
Colli W (2011) Organismos transgênicos no Brasil: regular ou desregular? Revista USP 89:148–173
De Clercq P, Mohaghegh J, Tirry L (2000) Effect of host plant on the functional response of the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Biol Control 18:65–70
Diez-Rodriguez GI, Omoto C (2001) Herança da resistência de Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) à lambda-cialotrina. Neotrop Entomol 30:311–316
Faria LDB, Godoy WAC, Trinca LA (2004) Dynamics of handling time and functional response by larvae of Chrysomya albiceps (Dipt., Calliphoridae) on different prey species. J Appl Entomol 128:432–436
Fok M (2011) Gone with transgenic cotton cropping in the USA. Biotechnol Agron Soc Environ 15:345–352
Freund RJ, Littell RC (1986) SAS system for regression. SAS Institute, Cary
Hagerty AM, Kilpatrick AL, Tumipseed SG, Sullivan ML (2005) Predaceous arthropods and lepidopteran pests on conventional, Bollgard, and Bollgard II cotton under untreated and disrupted conditions. Environ Entomol 34:105–114
Hassell MP (1978) The dynamics of arthropod predator-prey systems. Princeton University Press, Princeton
Hertlein MB, Thorarinsson K (1987) Variable patch times and the functional response of Leptopilina boulardi (Hymenoptera: Eucoilidae). Environ Entomol 16:593–598
Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398
Houck MA, Strauss RE (1985) A comparative study of functional responses: experimental design and statistical interpretation. Can Entomol 91:617–629
Huesing J, English L (2004) The impact of Bt crops on the developing world. AgBioForum 7:84–95
Institute Sas (2006) SAS/STAT user’s guide. SAS Institute, Cary
Juliano SA (1993) Nonlinear curve fitting: predation and functional response curves. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 159–182
Knipling EF (1980) Regional management of the fall armyworm: a realistic approach? Florida Entomol 63:468–480
Laycock A, Camm E, Van Laerhoven S, Gillespie D (2006) Cannibalism in a zoophytophagous omnivore is mediated by prey availability and plant substrate. J Insect Behav 19:219–229
Leibee GL, Capinera JL (1995) Pesticide resistance in Florida insects limits management options. Florida Entomol 78:386–399
Liu X, Chen M, Collins HL, Onstad D, Roush R, Zhang Q, Shelton AM (2012) Effect of insecticides and Plutella xylostella (Lepidoptera: Plutellidae) genotype on a predator and parasitoid and implications for the evolution of insecticide resistance. J Econ Entomol 105:354–362
Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365
Madadi H, Parizi EM, Allahyari H, Enkegaard A (2011) Assessment of the biological control capability of Hippodamia variegata (Col.: Coccinellidae) using functional response experiments. J Pest Sci 84:447–455
Malaquias JB, Ramalho FS, Fernandes FS, Souza JVS, Azeredo TL (2009) Effects of photoperiod on the development and growth of Podisus nigrispinus, a predator of cotton leafworm. Phytoparasitica 37:241–248
Malaquias JB, Ramalho FS, Fernandes FS, Nascimento JL Jr, Correia ET, Zanuncio JC (2010) Effects of photoperiod on reproduction and longevity of Podisus nigrispinus (Heteroptera: Pentatomidae). Ann Entomol Soc Am 103:603–610
Martinelli S, Clark PL, Zucchi MI, Silva MC, Foster JE, Omoto C (2007) Genetic structure and molecular variabillity of Spodoptera frugiperda (Lepidoptera: Noctuidae) collected in maize and cotton fields in Brazil. Bull Entomol Res 97:225–231
Medeiros RS, Ramalho FS, Serrão JE, Zanuncio JC (2004) Estimative of Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) development time with non linear models. Neotrop Entomol 33:141–148
Mohaghegh J, De Clercq P, Tirry L (2001) Functional response of the predators Podisus maculiventris (Say) and Podisus nigrispinus (Dallas) (Het., Pentatomidae) to the beet armyworm, Spodoptera exigua (Huëbner) (Lep., Noctuidae): effect of temperature. J Appl Entomol 125:131–134
Murdoch WW (1969) Switching in generalist predators: experiments on predator specificity and stability of prey populations. Ecol Monogr 39:335–354
Murdoch WW, Oaten A (1975) Predation and population stability. Adv Ecol Res 9:1–131
Nicholson AJ (1933) The balance of animal populations. J Anim Ecol 2:132–178
O’Neil RJ (1990) Functional response of arthropod predators and its role in the biological control of insect pests in agricultural systems. In Alan RL (ed.), New direction in biological control: alternatives for suppressing agricultural pests and diseases. West Lafayette: Purdue University, Indiana, pp 83–86
Pashley DP (1986) Host associated genetic differentiation in fall armyworm (Lepidoptera: Noctuidae): a sibling species complex? Ann Entomol Soc Am 79:898–904
Pereira AIA, Ramalho FS, Malaquias JB, Bandeira CM, Silva JES, Zanuncio JC (2008) Density of Alabama argillacea larvae affects food extraction by females of Podisus nigrispinus. Phytoparasitica 36:84–94
Pereira AIA, Ramalho FS, Rodrigues KCV, Malaquias JB, Souza JVS, Zanuncio JC (2010) Food extraction by the males of Podisus nigrispinus (Dallas) (Hemiptera: Pentatomidae) from cotton leafworm larvae. Braz Arch Biol Technol 53:1027–1035
Ramalho FS (1994) Cotton pest management. Part 4. A Brazilian perspective. Annu Rev Entomol 34:563–578
Ramalho FS, Azeredo TL, Nascimento ARB, Fernandes FS, Nascimento JR Jr, Malaquias JB, Domingues da Silva CA, Zanuncio JC (2011) Feeding of fall army worm, Spodoptera frugiperda, on Bt transgenic cotton and its isoline. Entomol Exp Appl 139:207–214
Randhawa GJ, Chhabra R (2013) Genetically modified cotton in India and detection strategies. Methods Mol Biol 958:17–28
Romeis J, van Driesche RG, Barrat BIP, Bigler F (2008) Insect resistant transgenic crops and biological control. In Romeis J, Shelton AM, Kennedy GG (eds.). Integration of insect-resistant genetically modified crops within IPM programs. Springer, Dordrecht, pp 87–118
Roush RT, Mckenzie JA (1987) Ecological genetics of insecticide and acaricide resistance. Annu Rev Entomol 32:361–380
Vivan LM, Torres JB, Veigas AFSL (2003) Development and reproduction of a predatory stinkbug, Podisus nigrispinus in relation to two different prey types and environmental conditions. Biocontrol 48:155–158
Wilkinson MJ, Ford CS (2007) Estimating the potential for ecological harm from gene flow to crop wild relatives. Biosafety Rev 3:42–63
Wu K, Mu W, Liang G, Guo Y (2005) Regional reversion of insecticide resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) is associated with the use of Bt cotton in northern China. Pest Manag Sci 61:497–498
Yu SJ (1992) Detection and biochemical characterization of insecticide resistance in fall armyworm (Lepidoptera: Noctuidae). J Econ Entomol 85:675–682
Zanuncio JC, Silva CAD, Rodrigues E, Pereira FF, Ramalho FS, Serrão JE (2008) Predation rate of Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae with and without defense by Podisus nigrispinus (Heteroptera: Pentatomidae). Braz Arch Biol Technol 51:125–129
Acknowledgments
The authors would like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the scholarships granted to the first author and also thank Embrapa Cotton for their technical support. Additional funds were received from the Brazilian agency Financiadora de Estudos e Projetos-FINEP.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by N. Desneux.
Rights and permissions
About this article
Cite this article
Malaquias, J.B., Omoto, C., Ramalho, F.S. et al. Bt cotton and the predator Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) in the management of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) resistance to lambda-cyhalothrin. J Pest Sci 88, 57–63 (2015). https://doi.org/10.1007/s10340-014-0585-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-014-0585-3