Abstract
In South America, especially in Brazil, four members of the Spodoptera complex, Spodoptera albula (Walker, 1857), S. cosmioides (Walker, 1858), S. eridania (Stoll, 1782), and S. frugiperda (J.E. Smith, 1797) are important pests of many crops, in particular corn, soybean and cotton crops. Spodoptera eridania and S. frugiperda have recently invaded Africa and caused serious crop damage, and S. frugiperda has invaded Asia and Oceania. The present study tested the effect of a range of seven temperatures (18–34 °C) on these four Spodoptera species simultaneously, assessing several biological variables. Based on the thermal tolerances obtained experimentally, the ecological zoning of each species in Brazil was mapped and compared spatially, according to the crop calendar of three important crops in different regions (first and second corn harvest, soybean and cotton). Our results showed that S. eridania had the lowest temperature threshold (Tt), i.e., it is favored in regions with more moderate temperatures; and did not tolerate the warmest temperature, failing to complete its development at 34 °C. In contrast, S. albula did not complete its development at 18 °C and may be more successful in warmer regions. In general, S. frugiperda and S. cosmioides were able to develop over a wide range of temperatures, and S. frugiperda showed a higher biological potential at all temperatures evaluated. Our biological data and the computational code are available online. The extensive data produced here can help other entomologists to delimit the spatial distribution of the Spodoptera complex and forecast outbreaks of these pests.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All datasets, R code, are made available as online supplementary materials, and software (algorithm) is available at 10.5281/zenodo.4594884.
References
Adamczyk JJ Jr, Sumerford DV (2000) Increased tolerance of fall armyworms (Lepidoptera: Noctuidae) to Cry1Ac δ-endotoxin when fed transgenic Bacillus thuringiensis cotton: impact on the development of subsequent generations. Fla Entomol 84:1–6. https://doi.org/10.2307/3496656
Almeida LP, Specht A, Teston JA (2013) Fauna of Noctuidae (Lepidoptera: Noctuoidea) in a pasture area in Altamira, Eastern Amazon, Pará, Brazil. Braz J Biol 74:983–990. https://doi.org/10.1590/1519-6984.07713
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Angulo A, Olivares T, Weigert G (2008) Estados inmaduros de lepidópteros nóctuidos de importancia agrícola y forestal en Chile y claves para su identificación (Lepidóptera: Noctuidae), 3rd edn. Universidad de Concepción, Concepción
Arnold CY (1959) The determination and significance of the base temperature in a linear heat unit system. J Am Soc Hortic Sci 74:430–445
Bean JL (1961) Predicting emergence of second-instar spruce budworm larvae from hibernation under field conditions in Minnesota. Ann Entomol Soc Am 54:175–177. https://doi.org/10.1093/aesa/54.2.175
Bernardi O, Sorgatto RJ, Barbosa AD, Domingues FA, Dourado PM, Carvalho RA, Martinelli S, Head GP, Omoto C (2014) Low susceptibility of Spodoptera cosmioides, Spodoptera eridania and Spodoptera frugiperda (Lepidoptera: Noctuidae) to genetically-modified soybean expressing Cry1Ac protein. Crop Prot 58:33–40. https://doi.org/10.1016/j.cropro.2014.01.001
Beserra EB, Parra JRP (2005) Impact of the number of Spodoptera frugiperda egg layers on parasitism by Trichogramma atopovirilia. Sci Agr 62:190–193. https://doi.org/10.1590/s0103-90162005000200016
Brasil (2016) Estudos, lista de cultivares indicadas para cada região e a relação de municípios com os respectivos calendários de plantio. Ministério da Agricultura, Pecuária e Abastecimentos. http://www.agricultura.gov.br/assuntos/riscos-seguro/risco-agropecuario/portarias Accessed 25 Jan 2020
Brito R, Specht A, Gonçalves GL, Moreira GRP, Carneiro E, Santos FL, Roque-Specht VF, Mielke OHH, Casagrande MM (2019) Spodoptera marima: a new synonym of Spodoptera ornithogalli (Lepidoptera: Noctuidae), with notes on adult morphology, host plant use and genetic variation along its geographic range. Neotrop Entomol 48:433–448. https://doi.org/10.1007/s13744-018-0654-z
Butt BA, Cantu E (1962) Sex determination of lepidopterous pupae, vol 1. USDA, Washington. https://doi.org/10.1017/CBO9781107415324.004
Cabezas MF, Nava DE, Geissler LO, Melo M, Garcia MS, Krüger R (2013) Development and leaf consumption by Spodoptera cosmioides (Walker) (Lepidoptera: Noctuidae) reared on leaves of agroenergy crops. Neotrop Entomol 42:588–594. https://doi.org/10.1007/s13744-013-0169-6
Campbell A, Frazer BD, Gilbert N, Gutierrez AP, Mackauer M (1974) Temperature requirements of someaphids and their parasites. J Appl Ecol 11:431–438. https://doi.org/10.2307/2402197
Carvalho RA, Omoto C, Field LM, Williamson MS, Bass C (2013) Investigating the molecular mechanisms of organophosphate and pyrethroid resistance in the fall armyworm Spodoptera frugiperda. PLoS ONE 8:e62268. https://doi.org/10.1371/journal.pone.0062268
Cruz I (1995) A lagarta-do-cartucho na cultura do milho. Embrapa Milho e Sorgo, Sete Lagoas, MG
Cruz I, Figueiredo MLC, Oliveira AC, Vasconcelos CA (1999) Damage of Spodoptera frugiperda (Smith) in different maize genotypes cultivated in soil under three levels of aluminium saturation. Int J Pest Manag 45:293–296. https://doi.org/10.1080/096708799227707
da Silva DM, Bueno AF, Stecca CS, Andrade K, Neves PMOJ, de Oliveira MCN (2017) Biology of Spodoptera eridania and Spodoptera cosmioides(Lepidoptera: Noctuidae) on different host plants. Fla Entomol 100:752–760. https://doi.org/10.1653/024.100.0423
da Silva IA, Oliveira GM, Lacerda LB, Batista JL, Lopes GN (2019) Perspectivas atuais da utilização de bioinseticidas em Spodoptera frugiperda (Lepidoptera: Noctuidae). Rev Bras Meio Ambiente 27:20–27. https://doi.org/10.5281/zenodo.3575253
EPPO (2019) EPPO A1 List of pests recommended for regulation as quarantine pests. European and Mediterranean Plant Protection Organization—EPPO https://www.eppo.int/ACTIVITIES/plant_quarantine/A1_list Accessed 15 June 2020
EPPO (2020) Spodoptera frugiperda detected in Northern Territory, Australia. European and Mediterranean Plant Protection Organization—EPPO https://gd.eppo.int/reporting/article-6749 Accessed 16 July 2020
ESRI (2018) ArcGIS desktop: version 10.3. Environmental Systems Research Institute, Redlands, CA
Fatoretto JC, Michel AP, Silva Filho MCS, Silva N (2017) Adaptive potential of fall armyworm (Lepidoptera: Noctuidae) limits Bt trait durability in Brazil. J Integr Pest Manag 8:1–10. https://doi.org/10.1093/jipm/pmx011
Favetti BM, Butnariu AR, Foerster LA (2015) Biology and reproductive capacity of Spodoptera eridania (Cramer) (Lepidoptera, Noctuidae) in different soybean cultivars. Rev Bras Entomol 59:89–95. https://doi.org/10.1016/j.rbe.2015.03.002
Ganiger PC, Yeshwanth HM, Muralimohan K, Vinay N, Kumar ARV, Chandrashekara K (2018) Occurrence of the new invasive pest, fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), in the maize fields of Karnataka. India Curr Sci 115:621–623
Garcia AG, Godoy WAC, Thomas JMG, Nagoshi RN, Meagher RL (2018) Delimiting strategic zones for the development of fall armyworm (Lepidoptera: Noctuidae) on corn in the State of Florida. J Econ Entomol 111:120–126. https://doi.org/10.1093/jee/tox329
Garcia AG, Ferreira CP, Godoy WAC, Meagher RL (2019) A computational model to predict the population dynamics of Spodoptera frugiperda. J Pest Sci 92:429–441. https://doi.org/10.1007/s10340-018-1051-4
Gazzoni DL, Yorinori JT (1995) Manual de identificação de pragas e doenças da soja. EMBRAPA, Brasília, DF
Goergen G, Kumar PL, Sankung SB, Togola A, Tamò M (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS ONE 11(10):e0165632. https://doi.org/10.1371/journal.pone.0165632
Greene GL, Leppla NC, Dickerson WA (1976) Velvetbean caterpillar: a rearing procedure and artificial medium. J Econ Entomol 69:487–488. https://doi.org/10.1093/jee/69.4.487
Haddad ML, Parra JRP, Moraes RCB (1999) Métodos para estimar os limites térmicos inferior e superior de desenvolvimento de insetos. FEALQ, Piracicaba, SP
Honék A (1996) Geographical variation in thermal requirements for insect development. Eur J Entomol 93:303–312
Kergoat GJ, Prowell DP, Le Ru BP, Mitchell A, Dumas P, Clamens AL, Condaminef FL, Silvain JF (2012) Disentangling dispersal, vicariance and adaptive radiation patterns: a case study using armyworms in the pest genus Spodoptera (Lepidoptera: Noctuidae). Mol Phylogenet Evol 65:855–870. https://doi.org/10.1016/j.ympev.2012.08.006
Knipling EF (1980) Regional management of the fall armyworm—a realistic approach? Fla Entomol 63:468–480. https://doi.org/10.2307/3494531
Lacerda LF, Coelho A Jr, Garcia AG, Sentelhas PC, Parra JRP (2019) Biology at different temperatures, thermal requirements, and ecological zoning of Opogona sacchari (Lepidoptera: Tineidae). J Econ Entomol 112:1676–1682. https://doi.org/10.1093/jee/toz103
Leppla NC (2009) The basics of quality control of insect rearing. In: Schneider JC (ed) Principles and procedures for rearing high quality insects. Mississippi State University, Starkville, MI, pp 289–304
Luginbill P (1928) The fall army worm. USDA Tech Bull. https://doi.org/10.22004/ag.econ.156281
Malaquias JB, Caprio MA, Godoy WAC, Omoto C, Ramalho FS, Pachú JKS (2020) Experimental and theoretical landscape influences on Spodoptera frugiperda movement and resistance evolution in contaminated refuge areas of Bt cotton. J Pest Sci 93:329–340. https://doi.org/10.1007/s10340-019-01145-1
McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall, London
Montezano DG, Specht A, Sosa-Gómez DR, Roque-Specht VF, Barros NM (2013) a) Biotic potential and reproductive parameters of Spodoptera eridania (Stoll) (Lepidoptera, Noctuidae) in the laboratory. Rev Bras Entomol 57:340–346. https://doi.org/10.1590/S0085-56262013005000026
Montezano DG, Specht A, Bortolin TM, Fronza E, Sosa-Gómez DR, Roque-Specht VF, Pezzi P, Luz PC, Barros NM (2013) b) Immature stages of Spodoptera albula (Walker) (Lepidoptera: Noctuidae): developmental parameters and host plants. Acad Bras Ciênc 85:271–284. https://doi.org/10.1590/s0001-37652013000100013
Montezano DG, Specht A, Sosa-Gómez DR, Roque-Specht VF, De Barros NM (2014) a) Immature stages of Spodoptera eridania (Lepidoptera: Noctuidae): developmental parameters and host plants. J Insect Sci 14:238. https://doi.org/10.1093/jisesa/ieu100
Montezano DG, Specht A, Sosa-Gómez DR et al (2014) b) Biotic potential, fertility and life table of Spodoptera albula (Walker) (Lepidoptera: Noctuidae), under controlled conditions. An Acad Bras Ciênc 86:723–732. https://doi.org/10.1590/0001-3765201402812
Montezano DG, Specht A, Sosa-Gómez DR, Roque-Specht VF, Malaquias JV, Paula-Moraes SV, Peterson JA, Hunt TE (2019) Biotic potential and reproductive parameters of Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae). J Agr Sci 11:240–252. https://doi.org/10.5539/jas.v11n13p240
Moral RA, Hinde J, Demétrio CGB (2017) Half-normal plots and overdispersed models in R: the hnp package. J Stat Softw 81:1–23. https://doi.org/10.18637/jss.v081.i10
Nagoshi RN (2009) Can the amount of corn acreage predict fall armyworm (Lepidoptera: Noctuidae) infestation levels in nearby cotton? J Econ Entomol 102:210–218. https://doi.org/10.1603/029.102.0130
Norris RF, Caswell-Chen EP, Kogan M (2003) Concepts in integrated pest management. Prentice Hall, Upper Saddle River, NJ
Parra JRP, Omoto C (2004) Cada vez mais terríveis. Cultivar 6:18–20
Parra JRP, Precetti AACM, Kasten P Jr (1977) Aspectos biológicos de Spodoptera eridania (Cramer, 1782) (Lepidoptera: Noctuidae) em soja e algodoeiro. An Soc Entomol Bras 6:147–155
Pogue M (2002) A world revision of the genus Spodoptera Guenée (Lepidoptera: Noctuidae). Mem Am Entomol Soc 43:1–202
R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: http://www.Rproject.org/
Sharanabasappa D, Kalleshwaraswamy CM, Asokan R, Swamy HMM, Maruthi MS, Pavithra HB, Hegde K, Navi S, Prabhu ST, Goergen G (2018) First report of the fall armyworm, Spodoptera frugiperda (J E Smith) (Lepidoptera: Noctuidae), an alien invasive pest on maize in India. Pest Manag Hort Ecosyst 24:23–29
Sparks AN (1979) A review of the biology of the fall armyworm. Fla Entomol 62:82–87. https://doi.org/10.2307/3494083
Specht A, Roque-Specht VF (2016) Immature stages of Spodoptera cosmioides (Lepidoptera: Noctuidae): developmental parameters and host plants. Zoologia 33:e20160053. https://doi.org/10.1590/S1984-4689zool-20160053
Specht A, Roque-Specht VF (2018) Biotic potential and reproductive parameters of Spodoptera cosmioides (Walker) (Lepidoptera: Noctuidae) in the laboratory. Braz J Biol 79:488–494. https://doi.org/10.1590/1519-6984.184595
Teodoro AV, Procopio SO, Bueno AF, Negrisoli Jr. AS, Carvalho HWL, Negrisoli CRCB, Brito LF, Guzzo EC (2013) Spodoptera cosmioides (Walker) e Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae): novas pragas de cultivos da região nordeste. Circular Técnica 131. EMBRAPA, Brasília, DF
Trudgill DL, Honèk A, Li D, Van Straalen NM (2005) Thermal time—concepts and utility. Ann Appl Biol 146:1–14. https://doi.org/10.1111/j.1744-7348.2005.04088.x
Vickery RA (1929) Studies on the fall army worm in the Gulf coast district of Texas. USDA Tech Bull 138:10–64
Westbrook JK, Nagoshi RN, Meagher RL, Fleischer SJ, Jairam S (2015) Modeling seasonal migration of fall armyworm moths. Int J Biometeorol 60:255–267. https://doi.org/10.1007/s00484-015-1022-x
Worner SP (1992) Performance of phenological models under variable temperature regimes: consequences of the Kaufmann or rate summation effect. Environ Entomol 21:689–699. https://doi.org/10.1093/ee/21.4.689
Acknowledgements
We would like to thank Neide Graciano Maria from USP/ESALQ for helping with rearing the Spodoptera species. We are grateful to the companies PROMIP and Biopartner for supplying us with the different species of Spodoptera. We also thank Janet Reid, JWR Associates, for revising and improving the English version of this article. AGG holds a fellowship awarded by FAPESP (19/26071-8).
Funding
São Paulo Research Foundation (FAPESP) (Process 2018/02317–5) as part of the São Paulo Advanced Research Center for Biological Control (SPARCBIO) hosted at the Luiz de Queiroz College of Agriculture (ESALQ) of the University of São Paulo (USP), sponsored by FAPESP, Koppert and USP. National Institute of Science and Technology Semiochemicals in Agriculture (INCT) (FAPESP 2014/50871–0/CNPq 465511/2014–7). Center for Agriculture and Bioscience International (CABI) project IC10001B—Invasive Best Practice Solutions (DGIS). CABI gratefully acknowledges the core financial support from CABI member countries (and lead agencies). See at https://www.cabi.org/about-cabi/who-we-work-with/key-donors/for full details.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
All applicable international, national and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.
Additional information
Communicated by Antonio Biondi .
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Parra, J.R.P., Coelho, A., Cuervo-Rugno, J.B. et al. Important pest species of the Spodoptera complex: Biology, thermal requirements and ecological zoning. J Pest Sci 95, 169–186 (2022). https://doi.org/10.1007/s10340-021-01365-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01365-4