Abstract
The cotton bollworm Helicoverpa armigera (Hübner) is a widespread lepidopteran pest found in various crops worldwide. This highly polyphagous species, commonly found both in the Old and New World, has caused significant economic damage as an invasive agricultural pest in Brazil since 2013. The goal of the present study is to provide a detailed morphological assessment of adults and immature stages of H. armigera, as this species is often confused with H. zea (Boddie), a congeneric species that is native to the New World. The biology data were acquired during four full life cycles, and observations on general behavior, nocturnal habits of larvae and adults, and sensitivity of larvae to humidity were recorded. Larval chaetotaxy differs between the first and the remaining instars, which bear L2 on the meso- and metathorax and L3 on A3 through A6, along with conspicuous chalazae and longitudinal bands. Important morphological characters of this species include the following: eggs with four micropylar openings, lined with 12 cells arranged in the shape of a rosette; pupa adecticous and obtect, with prominent spiracles; adults with the distal antennomere striate. Adults exhibit sexual dimorphism in the number of setae on the frenulum and spines on the prothoracic leg. Illustrations of the critical morphological features of this species are provided.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbasi B, Ahmed K, Khalique F, Ayub N, Liu H, Kazmi S, Aftab M (2007) Rearing the cotton bollworm, Helicoverpa armigera, on a tapioca-based artificial diet. J Insect Sci 7(35):1–7. https://doi.org/10.1673/031.007.3501
Ali A, Choudhury RA, Ahmad Z, Rahman F, Khan FR, Ahmad SK (2009) Some biological characteristics of Helicoverpa armigera on chickpea. Tunis J Plant Prot 4:99–106
Angulo AO, Olivares TS, Weigert GT (2006) Estados inmaduros de lepidópteros nóctuidos de importancia agrícola y forestal en Chile (Lepidoptera: Noctuidae). Universidad de Concepción, Concepción, p 154
Arnemann JA, James WJ, Walsh TK, Guedes JVC, Smagghe G, Castiglioni E, Tay WT (2016) Mitochondrial DNA COI characterization of Helicoverpa armigera (Lepidoptera: Noctuidae) from Paraguay and Uruguay. Genet Mol Res 15(2). doi:https://doi.org/10.4238/gmr.15028292
Assemi H, Rezapanah M, Vafaei-Shoushtari R, Mehrvar A (2012) Modified artificial diet for rearing of tobacco budworm, Helicoverpa armigera, using the Taguchi method and derringer’s desirability function. J Insect Sci 12(100):1–18. https://doi.org/10.1673/031.012.10001
Baker GT, Parrott WL, Jenkins JN (1986) Sensory receptors on the larval maxillae and labia of Heliothis zea (Boddie) and Heliothis virescens (F.) (Lepidoptera: Noctuidae). Int J Insect Morphol Embryol 15(3):227–232. https://doi.org/10.1016/0020-7322(86)90060-7
Bentivenha JPF, Paula-Moraes SV, Baldin ELL, Specht A, Silva IF, Hunt TE (2016) Battle in the New World: Helicoverpa armigera versus Helicoverpa zea (Lepidoptera: Noctuidae). PLoS One 11(12):e0167182. https://doi.org/10.1371/journal.pone.0167182
Blaik T, Malkiewicz A (2003) Morphology of larval and pupal stages of Isturgia roraria (Fabricius, 1777) (Lepidoptera: Geometridae). Ann Zool 53:245–258
Body BM, Daniels JC, Austin GT (2008) Predaceous behavior by Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae: Heliothinae). J Insect Behav 21(3):143–146. https://doi.org/10.1007/s10905-007-9113-0
Borges E, Faccioni-Heuser M, Moreira G (2010) Morphology of the prosternal glands of Heliconius erato (Lepidoptera: Nymphalidae). Psyche 1:8–8. https://doi.org/10.1155/2010/892960
Bueno AF, Sosa-Gómez DR (2014) The old world bollworm in the neotropical region: the experience of brazilian growers with Helicoverpa armigera. Outlooks Pest Manag 25(4):261–265. https://doi.org/10.1564/v25_aug_04
Butt BA, Cantu E (1962) Sex determination of lepidopterous pupae. Washington. USDA, p 7
CABI (2017) Invasive species compendium datasheets Helicoverpa armigera (cotton bollworm). Available in: http://www.cabi.org/isc/datasheet/26757. Accessed 8 May 2017
Callahan PS (1958) Serial morphology as a technique for determination of reproductive patterns in the corn earworm, Heliothis zea Boddie. Ann Entomol Soc Am 51(5):413–428. https://doi.org/10.1093/aesa/51.5.413
Casagrande MM (1979) Sobre Caligo beltrao (Illiger). IV: Morfologia externa do adulto - abdome (Lepidoptera, Satyridae, Brassolinae). Rev Bras Biol 39:711–716
Castiglioni E, Perini CR, Chiaravalle W, Arnemann JA, Ugalde G, Guedes JVC (2016) Primer registro de ocurrencia de Helicoverpa armigera (Hübner, 1808) (Lepidoptera: Noctuidae) en soja, en Uruguay. Agrocien Urug 20:31–35
Castrejón-Gómez VR, Valdez-Carrasco J, Cibrian-Tovar J, Camino-Lavin M, Osorio RO (1999) Morphology and distribution of the sense organs on the antennae of Copitarsia consueta (Lepidoptera: Noctuidae). Fla Entomol 82(4):546–555. https://doi.org/10.2307/3496472
Comstock JH (1918) The wings of the insects. Comstock Publishing Company, Nova Iorque, 430 p
Czepak C, Albernaz KC, Vivan LM, Guimarães HO, Carvalhais T (2013) Primeiro registro de ocorrência de Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) no Brasil. Pesqu Agropecu Trop 43(1):110–113. https://doi.org/10.1590/S1983-40632013000100015
Daly HV (1985) Insect morphometrics. Annu Rev Entomol 30(1):415–438. https://doi.org/10.1146/annurev.en.30.010185.002215
Diongue A, Yang J, Lai P (2013) Biomorphometric characteristics of different types of sensilla detected on the antenna of Helicoverpa armigera by scanning electron microscopy. J Asia Pac Entomol 16(1):23–28. https://doi.org/10.1016/j.aspen.2012.09.001
EMBRAPA (2013) Nota técnica sobre resultado do trabalho inicial de levantamento da lagarta do gênero Helicoverpa – detecção da espécie Helicoverpa armigera no Brasil. Technical Note 22 Mar 2013. Planaltina: EMBRAPA CERRADOS. 2 p. doi: https://doi.org/10.13140/RG.2.1.2946.7685
Feng H, Wu K, Cheng D, Guo Y (2004) Northward migration of Helicoverpa armigera (Lepidoptera: Noctuidae) and other moths in early summer observed with radar in northern China. J Econ Entomol 97:1874–1883. https://doi.org/10.1603/0022-0493-97.6.1874
Feng H, Gouldb F, Huang Y, Jiangd Y, Wua K (2010) Modeling the population dynamics of cotton bollworm Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) over a wide area in northern China. Ecol Model 221:1819–1830. https://doi.org/10.1016/j.ecolmodel.2010.04.003
Fibiger M, Lafontaine JD (2004) A review of the higher classification of the Noctuoidea (Lepidoptera) with special reference to the Holarctic fauna. Esper 11:7–690
Fitt GP (1989) The ecology of Heliothis species in relation to agroecosystems. Annu Rev Entomol 34(1):17–52. https://doi.org/10.1146/annurev.en.34.010189.000313
Forbes WTM (1916) On the tympanum of certain Lepidoptera. Psyche 23(6):183–192. https://doi.org/10.1155/1916/16801
Gilligan TM, Passoa SC (2014) LepIntercept—an identification resource for intercepted Lepidoptera larvae. Identification Technology Program (ITP), Fort Collins, CO 1:3
Gomez Rolim AAS, Yano SAC, Specht A, Andrade CGTJ, Sosa-Gómez DR (2013) Morphological and molecular characterization of the eggs of some noctuid species associated with soybean in Brazil. Ann Entomol Soc Am 106(5):643–651. https://doi.org/10.1603/AN13049
Grimes LR, Neuzing HH (1986) Morphological survey of the maxillae in last stage larvae of the suborder Ditrysia (Lepidoptera): Palpi. Ann Entomol Soc Am 79(3):491–509. https://doi.org/10.1093/aesa/79.3.491
Hallberg E, Hansson BS, Löfstedt C (2003) Sensilla and proprioceptors. In: Kristensen NP (ed) Lepidoptera, moths and butterflies. Vol.2: morphology, physiology and development. In: Fischer M (Ed.) Handbook of zoology. Vol, IV, Arthropoda:Insecta, vol 36. Walter de Gruyter, Berlin, New York, pp 267–288
Hamed M, Nadeem S (2008) Rearing of Helicoverpa Armigera (Hub.) on artificial diets in laboratory. Pak J Zool 40(6):447–450
Hardwick DF (1958) Taxonomy, life history and habits of the elliptoid-eyed species of Schinia, with notes on the Heliothidinae. Can Entomol 90(Suppl.6):1–116. https://doi.org/10.4039/entm9006fv
Hardwick DF (1965) The corn earworm complex. Mem Entomol (Soc Can 40):1–246
Hardwick DF (1970) A generic revision of the North American Heliothidinae (Lepidoptera: Noctuidae). Mem Entomol 102(Soc Can 73):1–59. https://doi.org/10.4039/entm10273fv
Hemming F (1937) Hübner: a bibliographical and systematic account of the entomological works of Jacob Hübner and of the supplements thereto by Carl Geyer. Gottfried Franz von Frölich and Gottlieb August Wilhelm Herrich-Schäffer. Royal Entomological Society of London, London, p 605
Hoy RR, Robert D (1996) Tympanal hearing in insects. Annu Rev Entomol 41(1):433–450. https://doi.org/10.1146/annurev.en.41.010196.002245
Jadhav DR, Armes NJ, Bhatnagar VS (2013) Incidence of winter and summer diapause in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Andhra Pradesh, India. Asian J Agric Sci 5(3):40–51
James DG, Hebert V, LePage J (2012) The prosternal gland in pacific northwest butterfly larvae with preliminary chemical analyses of emissions. J Lepid Soc 66(3):137–142. https://doi.org/10.18473/lepi.v66i3.a3
Jefferson RN, Rubin RE, McFarland SU, Shorey HH (1970) Sex pheromones of noctuid moths. XXII. The external morphology of the antennae of Trichoplusia ni, Heliothis zea, Prodenia ornithogalli, and Spodoptera exigua. Ann Entomol Soc Am 63(5):1227–1238. https://doi.org/10.1093/aesa/63.5.1227
Jones RW (1880) Boll worm devouring cotton worm. Am Entomol 3:253
Karim S (2000) Management of Helicoverpa armigera: a review and prospectus for Pakistan. Pak J Biol Sci 3(8):1213–1222
Kiriakoff SG (1963) The tympanic structure of the Lepidoptera and the taxonomy of the order. J Lepid Soc 17:1–20
Kitching IJ, Rawlins JE (1998) The noctuoidea. In: Kristensen NP (Ed.) Lepidoptera, moths and butterflies. Vol.1: evolution, systematic and biogeography. In: Fischer M (Ed.) Handbook of zoology. Vol. IV, Arthropoda:Insecta 35. Walter de Gruyter, Berlin, New York, pp. 355–401
Kristensen NP (2003) Reproductive organs. In: Kristensen, NP (Ed.) Lepidoptera, moths and butterflies. Vol.2: morphology, physiology and development. In: Fischer M (Ed.) Handbook of zoology. Vol. IV, Arthropoda:Insecta 36. Walter de Gruyter, Berlin, New York, pp. 427–447
Liu Z, Gong P, Li D, Wei W (2010) Pupal diapause of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) mediated by larval host plants: pupal weight is important. J Insect Physiol 56(12):1863–1870. https://doi.org/10.1016/j.jinsphys.2010.08.007
Matthews M (1991) Classification of the Heliothinae. Bull Nat Resour Inst 44:1–195
Mhatre N, Montealegre-Z F, Balakrishnan R, Robert D (2009) Mechanical response of the tympanal membranes of the tree cricket Oecanthus henryi. J Comp Physiol A 195(5):453–462. https://doi.org/10.1007/s00359-009-0423-x
Mironidis GK, Savopoulou-Soultani M (2008) Development, survivorship, and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) under constant and alternating temperatures. Environ Entomol 37(1):16–28.
Mitter C, Poole RW, Matthews M (1993) Biosystematics of the Heliothinae (Lepidoptera: Noctuidae). Annu Rev Entomol 38(1):207–225. https://doi.org/10.1146/annurev.en.38.010193.001231
Monsalve S, Dombroskie JJ, Lam WHY, Rota J, Brown JW (2011) Variation in the female frenulum in Tortricidae (Lepidoptera). Part 3. Tortricinae. Proc Entomol Soc Wash 113(3):335–370. https://doi.org/10.4289/0013-8797.113.3.335
Montezano DG, Specht A, Bortolin TM, Fronza E, Sosa-Gómez DR, Roque-Specht VF, Pezzi P, Luz PC, Barros NM (2013) Immature stages of Spodoptera albula (Walker) (Lepidoptera: Noctuidae): developmental parameters and host plants. An Acad Bras Cienc 85(1):271–284. https://doi.org/10.1590/S0001-37652013000100013
Mosher E (1916) A classification of the Lepidoptera based on characters of the pupae. Bull Ill State Lab Nat Hist 12:17–159
Murúa MG, Scalora FS, Navarro FR, Cazado LE, Casmuz A, Villagrán ME, Lobos E, Gastaminza G (2014) First record of Helicoverpa armigera (Lepidoptera: Noctuidae) in Argentina. Fla Entomo 97(2):854–856. https://doi.org/10.1653/024.097.0279
Nadda G (2013) Medicinal and aromatic crops as hosts of Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). Lepcey - J Trop Asian Entomol 02(1):44–46
Peterson A (1961) Some types of eggs deposited by moths, Heterocera-Lepidoptera. Fla Entomo 44(3):107–114. https://doi.org/10.2307/3492966
Peterson A (1962) Larvae of insects. An introduction to Neartic species. Part I. Lepidoptera and plant infesting Hymenoptera. Edwards Brothers, Ann Arbor, Michigan, p. 315
Peterson A (1964) Egg types among moths of the Noctuidae (Lepidoptera). Fla Entomo 47(2):71–91. https://doi.org/10.2307/3493280
Pierce FN (1909) The genitalia of the group Noctuidae of the Lepidoptera of the British Islands. Liverpool, A.W. Duncan, p. 88
Rajaei H, Greve C, Letsch H, Stüning D, Wahlberg N, Minet J, Misof B (2015) Advances in Geometroidea phylogeny, with characterization of a new family based on Pseudobiston pinratanai (Lepidoptera, Glossata). Zool Scr 44(4):418–436. https://doi.org/10.1111/zsc.12108
Rota J, Yang A, Brown JW (2009) Variation in the female frenulum in Tortricidae (Lepidoptera). Part 2. Olethreutinae. Proc Entomol Soc Wash 111(4):826–866. https://doi.org/10.4289/0013-8797-111.4.826
Scoble M (1992) The Lepidoptera. Form, function and diversity. Natural History Museum Publications. Oxford University Press, London, p 404
Seada MA (2015) Antennal morphology and sensillum distribution of female cotton leaf worm Spodoptera littoralis (Lepidoptera: Noctuidae). J Basic Appl Zool 68:10–18. https://doi.org/10.1016/j.jobaz.2015.01.005
SENAVE (2013) Senave en alerta tras ingreso de peligrosa plaga agrícola. Available in: http://www.abc.com.py/edicion-impresa/economia/senave-en-alerta-tras-ingreso-de-peligrosa-plaga-agricola-629240.html. Accessed 17 Oct 2013
Snodgrass RE (1935) Principles of insect morphology. McGraw-Hill Book Company, Nova York, p 665
Sorensen GS, Cribb BW, Merritt D, Johnson ML, Zaluck MP (2006) Structure and ultrastructure of the silk glands and spinneret of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Arthropod Struct Dev 35(1):3–13. https://doi.org/10.1016/j.asd.2005.10.002
Sosa-Gómez DR, Specht A, Paula-Moraes SV, Lopes-Lima A, Yano SAC, Micheli A, Morais EGF, Gallo P, Pereira PRVS, Salvadori JR, Botton M, Zenker MM, Azevedo-Filho WS (2016) Timeline and geographical distribution of Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae: Heliothinae) in Brazil. Rev Bras Entomol 60(1):101–104. https://doi.org/10.1016/j.rbe.2015.09.008
Specht A, Formentini AC, Corseuil E (2006) Biologia de Automeris illustris (Walker) (Lepidoptera, Saturniidae, Hemileucinae). Rev Bras Zool 23(2):537–546. https://doi.org/10.1590/S0101-81752006000200029
Specht A, Sosa-Gómez DR, Paula-Moraes SV, Yano SAC (2013) Helicoverpa armigera (Lepidoptera: Noctuidae: Heliothinae) no Brasil: Identificação morfológica e molecular. Pesqu Agropecu Bras 48(6):689–692. https://doi.org/10.1590/S0100-204X2013000600015
Speidel W, Fänger H, Naumann CM (1996) The phylogeny of the Noctuidae (Lepidoptera). Syst Entomol 21(3):219–251. https://doi.org/10.1046/j.1365-3113.1996.d01-14.x
Stehr FW (1987) Order Lepidoptera. In: Stehr FW (Ed.) Immature insects. Kendall/Hunt, Dubuque, Iowa, pp. 288–596
Tay WT, Soria MF, Walsh T, Thomazoni D, Silvie P, Behere GT, Anderson C, Downes S (2013) A brave new world for an old world pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS One 8(11):e80134. https://doi.org/10.1371/journal.pone.0080134
Vegliante F, Hasenfuss I (2012) Morphology and diversity of exocrine glands in lepidopteran larvae. Annu Rev Entomol 57(1):187–204. https://doi.org/10.1146/annurev-ento-120710-100646
Wang HL, Ming QL, Zhao CH, Wang CZ (2008) Genetic basis of sex pheromone blend difference between Helicoverpa armigera (Hübner) and Helicoverpa assulta (Gueneée) (Lepidoptera: Noctuidae). J Insect Physiol 54(5):813–817. https://doi.org/10.1016/j.jinsphys.2008.02.011
Yang A, Brown JW (2009) Variation in the female frenulum in Tortricidae (Lepidoptera). Part 1. Chlidanotinae. Proc Entomol Soc Wash 111(3):742–750. https://doi.org/10.4289/0013-8797-111.3.743
Zalucki MP, Daglish G, Firempong S, Twine P (1986) The biology and ecology of Heliothis armigera (Hübner) and H. punctigera Wallengren (Lepipoptera: Noctuidae) in Australia: what do we know? Aust J Zool 34(6):779–814. https://doi.org/10.1071/ZO9860779
Acknowledgments
Illustrations presented in this paper were acquired at the Electron Microscopy Center (CEM-UFPR) and Taxonline at Universidade Federal do Paraná, Curitiba, Brazil. The authors thank Dr. Fernando Dias Maia for assisting with image editing and Olivia Evangelista, Ana Dal Molin, and Keith Bayless for translating and proofreading an earlier version of this manuscript. We also thank Dr. Daniel R. Sosa-Gómez (Embrapa Soja, Londrina, Paraná, Brazil) for sending the pupae. Thanks again to Takumasa Kondo, and three anonymous reviewers, for detailed comments and corrections that improved this paper.
Funding
This research was funded by the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq) (LQS proc. no. 130624/2014-1; MMC proc. no. 308247/2013-2; AS proc. no. 403376/2013-0, 476691/2013-3, 47304/2013-8) and Embrapa (proc. SEG MP2 - 02.13.14.006.00.00).
Author information
Authors and Affiliations
Corresponding author
Additional information
Edited by Takumasa Kondo – CORPOICA
Rights and permissions
About this article
Cite this article
Queiroz-Santos, L., Casagrande, M.M. & Specht, A. Morphological Characterization of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae: Heliothinae). Neotrop Entomol 47, 517–542 (2018). https://doi.org/10.1007/s13744-017-0581-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-017-0581-4