Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-19T05:38:45.672Z Has data issue: false hasContentIssue false

Role of nutritional composition in the development and survival of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) on artificial diet and natural hosts

Published online by Cambridge University Press:  18 August 2020

Ivana F. da Silva*
Affiliation:
Universidade Estadual Paulista, Faculdade de Ciências Agronômicas, Departamento de Proteção Vegetal, Botucatu, São Paulo, Brasil18610-034, Brazil
Edson Luiz L. Baldin
Affiliation:
Universidade Estadual Paulista, Faculdade de Ciências Agronômicas, Departamento de Proteção Vegetal, Botucatu, São Paulo, Brasil18610-034, Brazil
Alexandre Specht
Affiliation:
Embrapa Cerrados, BR 020 Km 18, Planaltina, Distrito Federal, Brasil73310-970, Brazil
Vânia F. Roque-Specht
Affiliation:
Universidade de Brasília, Planaltina, Distrito Federal, Brasil73345-010, Brazil
Rafaela Morando
Affiliation:
Universidade Estadual Paulista, Faculdade de Ciências Agronômicas, Departamento de Proteção Vegetal, Botucatu, São Paulo, Brasil18610-034, Brazil
Juaci V. Malaquias
Affiliation:
Embrapa Cerrados, BR 020 Km 18, Planaltina, Distrito Federal, Brasil73310-970, Brazil
Silvana V. Paula-Moraes
Affiliation:
University of Florida, West Florida Research and Education Center, 4253 Experiment Road, JayFL32565, USA
*
Author for correspondence: Ivana F. da Silva, Email: ivanaf.silva@hotmail.com

Abstract

Helicoverpa armigera is a pest of several crops causing significant economic impact. We evaluated the insect development on different vegetative and reproductive structures of cotton, maize, and soybean compared to artificial diet. One hundred individuals were evaluated per structure (cotton leaves and bolls; maize leaves, grains, and silk; soybean leaves and pods) and artificial diet. Centesimal analyses were performed on quantifiable nutrient contents in diets. The viability of immatures (eggs, larvae, and pupae) ranged from 30% on maize leaf to 74% on cotton bolls, while on the artificial diet, it was 70%. Maize, cotton, and soybean leaves provided viability of 30, 37, and 42%, respectively, revealing these leaves tissues are less favorable to the development of H. armigera immatures compared to ‘reproductive tissues’. Centesimal composition of diets compared 14 common components in all diets, which correlated significantly with larval and pupal stages and/or pupal weight. Of the 12 dietary components that significantly affected larval development time, half were negatively correlated, indicating a decrease in developmental time from their increments. In general, when insects were confined separately to substrates, the artificial diet was the most suitable for H. armigera development compared to the evaluated natural diets. However, in natural conditions, the variability of available hosts must be considered. In addition, it is acceptable for moths to select more suitable hosts for oviposition, while their larvae move to other more suitable tissues of the same plant or even migrate to other plants.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

AOAC (2010) Official Methods of Analysis of Association of Official Analytical Chemists. Horwitz W and Latimer G (eds). 18th Edition - Revision 3. Maryland/USA: AOAC, 72p.Google Scholar
Awmack, CS and Leather, SR (2002) Host plant quality and fecundityin herbivorous insects. Annual Review of Entomology 47, 817844.CrossRefGoogle ScholarPubMed
Azambuja, R, Degrande, PE, dos Santos, RO, Souza, EP and Gomes, CEC (2015) Effect of Bt soybean on larvae of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Journal of Agricultural Science 7, 9094.CrossRefGoogle Scholar
Barbosa, TAN, Mendes, SM, Rodrigues, GT, Ribeiro, PEA, Santos, CA, Valicente, FH and Oliveira, CM (2016) Comparison of biology between Helicoverpa zea and Helicoverpa armigera (Lepidoptera: Noctuidae) reared on artificial diets. Florida Entomologist 99, 7276.CrossRefGoogle Scholar
Barros, E, Torres, JB, Ruberson, JR and Oliveira, MD (2010) Development of Spodoptera frugiperda on different hosts and damage to reproductive structures in cotton. Entomologia Experimentalis et Applicata 137, 237245.CrossRefGoogle Scholar
Behmer, ST (2009) Insect herbivore nutrient regulation. Annual Review of Entomology 54, 165187.CrossRefGoogle ScholarPubMed
Bentivenha, JPF, Paula-Moraes, SV, Baldin, ELL, Specht, A, Silva, IF and Hunt, TE (2016) Battle in the new world: Helicoverpa armigera versus Helicoverpa zea (Lepidoptera: Noctuidae). PLoS ONE 11, e0167182.CrossRefGoogle Scholar
Bernarys, EA and Singer, M (2002) Contrasted foraging tactics in two species of polyphagous caterpillars. Acta Zoologica Academiae Scientiarum Hungaricae 48, 117135.Google Scholar
Bisht, K, Verma, S and Singh, NN (2018) Comparison of enhanced artificial diets for mass rearing of Helicoverpa armigera (Hubner) under laboratory conditions. Journal of Entomology and Zoology Studies 6, 25512553.Google Scholar
Coelho, AM and França, GE (1995) Seja o doutor do seu milho: nutrição e adubação. 2 ed. Informações Agronômicas. Arquivo do Agrônomo de Piracicaba, 71, 19.Google Scholar
Cohen, AC (2015) Insect Diets: Science and Technology. New York: CRC Press Second, 324p.CrossRefGoogle Scholar
Cohen, AC and Crittenden, P (2004) Deliberately added and ‘cryptic’ antioxidants in three artificial diets for insects. Journal of Economic Entomology 97, 265272.CrossRefGoogle ScholarPubMed
Cunningham, JP and Zalucki, MP (2014) Understanding heliothine (Lepidoptera: Heliothinae) pests: what is a host plant? Journal of Economic Entomology 107, 881896.CrossRefGoogle ScholarPubMed
Czepak, C, Albernaz, KC, Vivan, LM, Guimarães, HO and Carvalhais, T (2013) Primeiro registro de ocorrência de Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) no Brasil. Pesquisa Agropecuária Tropical 43, 110113.CrossRefGoogle Scholar
Embrapa (1999) Sistema Brasileiro de Classificação de Solos. Rio de Janeiro: Embrapa Solos, 412p.Google Scholar
FDA Food and Drung (2010) Administration. Elemental analysis manual. United States of America. Section 4, 4. Inductively coupled plasma? Atomic emission spectrometric determination of elements in food using microwave assisted digestion.Google Scholar
Fefelova, AY and Frolove, AN (2008) Distribution and mortality of corn earworm (Helicoverpa armigera, Lepidoptera, Noctuidae) on corn plants in Krasnodar territory. Entomological Review 88, 480484.CrossRefGoogle Scholar
Hemati, SA, Naseri, B, Nouri-Ghanbalani, G, Rafiee-Dastjerdi, H and Golizadeh, A (2012) Effect of different host plants on nutritional indices of the pod borer Helicoverpa armigera. Journal of Insect Science 12, 115.CrossRefGoogle ScholarPubMed
Hoffmann-Campo, CBH, Oliveira, EB and Moscardi, F (1985) Criação massal da lagarta da soja (Anticarsia gemmatalis). Londrina: Embrapa Soja, 23p.Google Scholar
Honnakerappa, SB and Udikeri, SS (2018) Abundance of Helicoverpa armigera (Hubner) on different host crops. Journal of Farm Science 31, 436439.Google Scholar
Hosseininejad, AS, Naseri, B and Razmjou, J (2015) Comparative feeding performance and digestive physiology of Helicoverpa armigera (Lepidoptera: Noctuidae) larvae-fed 11 corn hybrids. Journal of Insect Science 15, 16.CrossRefGoogle ScholarPubMed
Huang, J, Yu, Z, Gao, H, Yan, X, Chang, J, Wang, C, Hu, J and Zhang, L (2017) Chemical structures and characteristics of animal manures and composts during composting and assessment of maturity indices. PLoS ONE 12(6), e0178110.CrossRefGoogle ScholarPubMed
Kennedy, GG and Storer, NP (2000) Life systems of poplyphagous arthropod pests in temporally unstable cropping systems. Annual Review of Entomology 45, 467493.CrossRefGoogle ScholarPubMed
Krishnareddy, B and Hanur, VS (2015) Enhanced synthetic diet for rearing H. armigera under laboratory conditions. Journal of Entomology and Zoology Studies 3, 165167.Google Scholar
Kriticos, DJ, Ota, N, Hutchison, WD, Beddow, J, Walsh, T, Tay, WT, Borchert, DM, Paula-Moreas, SV, Czepak, C and Zalucki, MP (2015) The potential distribution of invading Helicoverpa armigera in North America: is it just a matter of time? PLoS ONE 10, e0119618.CrossRefGoogle ScholarPubMed
Kumar, S and Saini, RK (2008) Feeding preference and damage potential of Helicoverpa armigera (Hübner) on different promising cotton genotypes/hybrid. Journal of Agricultural Science and Technology 10, 411420.Google Scholar
Kumar, S, Saini, RK and Ram, P (2009) Natural mortality of Helicoverpa armigera (Hübner) eggs in the cotton ecosystem. Journal of Agricultural Science and Technology 11, 1725.Google Scholar
Liu, ZD, Li, DM, Gong, PY and Wu, KJ (2004) Life table studies of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), on different host plants. Environmental Entomology 33, 15701576.CrossRefGoogle Scholar
Liu, Z, Gong, P, Heckel, DG, Wei, W, Sun, J and Li, D (2009) Effects of larval host plants on over-wintering physiological dynamics and survival of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Journal of Insect Physiology 55, 19.CrossRefGoogle Scholar
Maelzer, DA and Zalucki, MP (1999) Analysis and interpretation of long-term light trap data for Helicoverpa spp. (Lepidoptera: Noctuidae) in Australia: the effect of climate and crop host plants. Bulletin of Entomological Research 89, 455464.CrossRefGoogle Scholar
Marur, CJ and Ruano, O (2001) A reference system for determination of developmental stages of upland cotton. Revista Brasileira de Oleaginosas e Fibrosas 5, 313317.Google Scholar
Montezano, DG, Specht, A, Sosa-Gómez, DR, Roque-Specht, VF, Malaquias, JV, Paula-Moraes, SV, Peterson, JA and Hunt, TE (2019) Biotic potential and reproductive parameters of Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae). Journal of Agricultural Science 11, 240252.CrossRefGoogle Scholar
Moreau, J, Benrey, B and Thiery, D (2006) Assessing larval food quality for phytophagous insects: are the facts as simple as they appear? Functional Ecology 20, 592600.CrossRefGoogle Scholar
Naseri, B and Razmjou, J (2013) Effect of artificial diets containing different corn hybrids powdered seeds on digestive proteolytic and amylolytic activities and nutritional responses of Helicoverpa armigera (Lep.: Noctuidae). Applied Entomology and Zoology 80, 918.Google Scholar
Naseri, B, Fathipour, Y, Moharramipour, S and Hosseininaveh, V (2009) Life table parameters of the cotton bollworm, Helicoverpa armigera (Lep: Noctuidae) on different soybean cultivars. Journal of Entomological Science 29, 2540.Google Scholar
Naseri, B, Fathipour, Y, Moharramipour, S and Hosseininaveh, V (2011) Comparative reproductive performance of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) reared on thirteen soybean varieties. Journal of Agricultural Science and Technology 13, 1726.Google Scholar
Parra, JRP (2009) A evolução das dietas artificiais e suas interações em ciência e tecnologia. In Panizzi AR and Parra JRP (eds) Bioecologia e nutrição de insetos: base para o manejo integrado de Pragas. Brasília, DF: Embrapa Informação Tecnológica, pp. 91174.Google Scholar
Parra, JRP, Panizzi, AR and Haddad, ML (2009) Índices nutricionais para medir consumo e utilização de alimentos por insetos. In Panizzi AR and Parra JRP (eds) Bioecologia e nutrição de insetos: base para o manejo integrado de Pragas. Brasília, DF: Embrapa Informações Tecnológicas, pp. 3790.Google Scholar
Paula-Moraes, SV, Silva, FMA and Specht, A (2017) Options and challenges for pest control in intensive cropping systems in tropical regions. In Rapisarda, C and Cocuzza, GEM (eds), Integrated Pest Management in Tropical Regions, Italy: CABI, Università degli Studi di Catania, 347p.Google Scholar
Pereira, RR, Neves, DVC, Campos, JN, Santana Júnior, PA, Hunt, TE and Picanço, MC (2018) Natural biological control of Chrysodeixis includens. Bulletin of Entomological Research 108, 112.CrossRefGoogle ScholarPubMed
Perkins, LE, Cribb, BW, Hanan, J and Zalucki, MP (2009) The role of two plant-derived volatiles in the foraging movement of 1st instar Helicoverpa armigera (Hübner): time to stop and smell the flowers. Arthropod-Plant Interactions 3, 173179.CrossRefGoogle Scholar
Petit, C, Ahuya, P, Le, RB, Kaiser-Arnauld, L, Harry, M and Calatayud, PA (2018) Odour and feeding preference of noctuid moth larvae conditioned to vanillin diet and non-vanillin diet. Phytoparasitica 46, 223232.CrossRefGoogle Scholar
Pogue, MG (2004) A new synonym of Helicoverpa zea (Boddie) and differentiation of adult males of H. zea and H. armigera (Hübner) (Lepidoptera: Noctuidae: Heliothinae). Annals of the Entomological Society of America 97, 12221226.CrossRefGoogle Scholar
Queiroz-Santos, L, Casagrande, MM and Specht, A (2018) Morphological characterization of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae: Heliothinae). Neotropical Entomology 47, 517542.CrossRefGoogle Scholar
Rahimi Namin, F, Naseri, B and Razmjou, J (2014) Nutritional performance and activity of some digestive enzymes of the cotton bollworm, Helicoverpa armigera, in response to seven tested bean cultivars. Journal of Insect Science 14, 118.CrossRefGoogle Scholar
Razmjou, J, Naseri, B and Hemati, SA (2014) Comparative performance of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) on various host plants. Journal of Pest Science 87, 2937.CrossRefGoogle Scholar
RDC360/2003 – BRASIL. Resolução RCD n° 360, 2003. Aprova regulamento técnico sobre rotulagem nutricional de alimentos embalados, tornando obrigatória a rotulagem nutricional, da Agência Nacional de Vigilância Sanitária. Diário oficial, Brasília.Google Scholar
Reigada, C, Guimarães, KF and Parra, JRP (2016) Relative fitness of Helicoverpa armigera (Lepidoptera: Noctuidae) on seven host plants: a perspective for IPM in Brazil. Journal of Insect Science 16, 15.CrossRefGoogle ScholarPubMed
Ritchie, S and Hanway, JJ (1989) How a corn plant develops. Ames: Iowa State University of Science and Technology, Coop. Ext. Serv. (Special Report, 48).Google Scholar
Ritchie, S, Hanway, JJ and Thompson, HE (1982) How a soybean plant develops. Ames: Iowa State University of Science and Technology, Coop. Ext. Serv. (Special Report, 53).Google Scholar
Ruan, YM and Wu, KJ (2001) Performances of the cotton bollworm, Helicoverpa armigera on different food plants. Acta Entomologica Bohemoslovaca 44, 205212.Google Scholar
Sarate, PJ, Tamhane, VA, Kotkar, HM, Ratnakaran, N, Susan, N, Gupta, VS and Giri, AP (2012) Developmental and digestive flexibilities in the midgut of a polyphagous pest, the cotton bollworm, Helicoverpa armigera. Journal of Insect Science 12, 42.CrossRefGoogle ScholarPubMed
Schellhorn, NA, Pierce, S, Bianchi, FJJA, Williams, D and Zalucki, MP (2008) Designing landscapes for multiple outcomes in broadacre environments. Australian Journal of Experimental Agriculture 48, 15491559.CrossRefGoogle Scholar
Scott, LJ, Lawrence, N, Lange, CL, Graham, GC, Hardwick, S, Rossiter, L, Dillon, ML and Scott, KD (2006) Population dynamics and gene flow of Helicoverpa armigera (Lepidoptera: Noctuidae) on cotton and grain crops in the Murrumbidgee Valley, Australia. Annals of the Entomological Society of America 99, 155163.Google ScholarPubMed
Scriber, JM and Slansky, F (1981) The nutritional ecology of immature insects. The Annual Review of Entomology 26, 183211.CrossRefGoogle Scholar
Siegel, S and Castellan, JNJ (2006) Estatística não-paramétrica para ciências do comportamento, 2nd Edn. Porto Alegre: Artmed, 448p.Google Scholar
Silva, IF, Baldin, ELL, Specht, A, Sosa-Gómez, DR, Roque-Specht, VF, Morando, R and Paula-Moraes, SV (2017) Biotic potential and life table of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) from three Brazilian regions. Neotropical Entomology 47, 344351.CrossRefGoogle ScholarPubMed
Silva, IF, Baldin, ELL, Specht, A, Sosa-Gomez, DR, Roque-Specht, VF, Morando, R and Paula-Morais, SV (2018) Biological and molecular characterization of the post invasion immature stages of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Florida Entomologist 101, 2532.CrossRefGoogle Scholar
Silveira Neto, S, Nakano, O, Barbin, D and Villa Nova, NA (1976) Manual de ecologia dosinsetos. São Paulo: Agronômica Ceres, 419p.Google Scholar
Soleimannejad, S, Fathipour, Y, Moharramipour, S and Zalucki, MP (2010) Evaluation of potential resistance in seeds of different soybean cultivars to Helicoverpa armigera (Lepidoptera: Noctuidae) using demographic parameters and nutritional indices. Journal of Economic Entomology 103, 14201430.CrossRefGoogle ScholarPubMed
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 and Azevedo-Filho, WS (2016) Timeline and geographical distribution of Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae: Heliothinae) in Brazil. Revista Brasileira de Entomologia 60, 101104.CrossRefGoogle Scholar
Specht, A, Sosa-Gómez, DR, Paula-Moraes, SVD and Yano, SAG (2013) Identificação morfológica e molecular de Helicoverpa armigera (Lepidoptera: Noctuidae) e ampliação de seu registro de ocorrência no Brasil. Pesquisa Agropecuária Brasileira 48, 689692.CrossRefGoogle Scholar
Specht, A, Montezano, DG, Sosa-Gómez, DR, Paula-Moraes, SV, Roque-Specht, VF and Barros, NM (2016) Reproductive potential of Spodoptera eridania (Stoll) (Lepidoptera: Noctuidae) in the laboratory: effect of multiple couples and the size. Brazilian Journal of Biology 76, 526530.CrossRefGoogle ScholarPubMed
Suzana, CS, Damiani, R, Fortuna, LS and Salvadori, JR (2015) Desempenho de larvas de Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) em diferentes fontes alimentares. Pesquisa Agropecuária Tropical 45, 480485.CrossRefGoogle Scholar
Tisdale, RA and Sappington, TW (2001) Realized and potential fecundity, egg fertility, and longevity of laboratory-reared female beet armyworm (Lepidoptera: Noctuidae) under different adult diet regimes. Annals of the Entomological Society of America 94, 415419.CrossRefGoogle Scholar
Wang, P, Furlong, MJ, Walsh, TK and Zalucki, MP (2019) Moving to keep fit: feeding behavior and movement of Helicoverpa armigera (Lepidoptera: Noctuidae) on artificial diet with different protein: carbohydrate ratios. Journal of Insect Science 19, 19.CrossRefGoogle ScholarPubMed
Yamasaki, A and Fujisaki, K (2010) Larval feeding preference and performance of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), on different flower parts of cosmos. Applied Entomology and Zoology 45, 627633.CrossRefGoogle Scholar
Yue, Z, Liu, X, Zhou, Z, Hou, G, Hua, J and Zhao, Z (2016) Development of a novel-type transgenic cotton plant for control of cotton bollworm. Plant Biotechnology Journal 14, 19.CrossRefGoogle ScholarPubMed
Zalucki, MP and Furlong, MJ (2005) Forecasting Helicoverpa populations in Australia: a comparison of regression based models and a bioclimatic based modelling approach. Insect Science 12, 4556.CrossRefGoogle Scholar
Zalucki, MP, Daglish, G, Firempong, S and Twine, P (1986) The biology and ecology of Heliothis armigera (Hübner) and Heliothis punctigera Wallengren (Lepidoptera: Noctuidae) in Australia: what do we know? Australian Journal of Zoology 34, 779814.CrossRefGoogle Scholar
Zalucki, MP, Murray, D, Gregg, P, Fitt, G, Twine, P and Jones, C (1994) Ecology of Helicoverpa armigera (Hübner) and Heliothis punctigera (Wallengren) in the Inland of Australia: larval sampling and host-plant relationship during winter and spring. Australian Journal of Zoology 42, 329346.CrossRefGoogle Scholar
Zalucki, MP, Clarke, AR and Malcolm, SB (2002) Ecology and behavior of first instar larval Lepidoptera. Annual Review of Entomology 47, 361393.CrossRefGoogle ScholarPubMed