Effect of host plant cultivar and nitrogen fertilization on life history of Helicoverpa armigera (Lepidoptera: Noctuidae)
Fereshteh Salehi 1, C  
Gholamhossein Gharekhani 1, A,C,E-F
Jalal Shirazi 2, C,E-F
Nahid Vaez 3, B
More details
Hide details
Department of Plant Protection, Faculty of Agriculture, University of Maragheh, Maragheh, Iran
Deparment of Agricultural Entomology, Iranian Research Institute of plant Protection, Tehran, Iran
Department of Plant Protection, Faculty of Agriculture, Azarbaijan Shahid Madani University, Azarbaijan, Iran
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
Fereshteh Salehi   

Department of Plant Protection, Faculty of Agriculture, University of Maragheh, 12, 021, Tehran, Iran
Online publication date: 2020-06-10
Submission date: 2019-07-30
Acceptance date: 2019-12-09
Journal of Plant Protection Research 2020;60(2):161–175
The current survey was carried out to evaluate the effect of different nitrogen levels (0, 2.1, 3.0, 3.9 g ∙ pot–1 nitrogen as urea 46%) on tomato fruit worm Helicoverpa armigera on six common tomato cultivars (e.g., Kingston, Riogrand, Earlyurbana, Redston, Superstrain-B and Primoearly) under laboratory conditions [25 ± 1°C, 60 ± 5% RH, 16 : 8 (L : D) h]. The mortality, developmental period of immature stages as well as the longevity and fecundity of adult stages were recorded. Data were analyzed based on the age-stage, two-sex lifetable theory. The longest (24.21 ± 0.59 days) larval developmental period was recorded in Earlyurbana variety with zero nitrogen level and the shortest (15.44 ± 0.36 days) in Superstrain-B variety with the highest nitrogen level. Consequently, the net reproductive rate (R0) ranged from 35.7 ± 7.06 to 62.16 ± 18.9 offspring/female/individual in Redston variety with zero nitrogen level and in Superstrain-B variety with the highest nitrogen level, respectively. The lowest and highest values of the intrinsic rate (r) and finite rate of increase (l) were estimated for Redston variety with zero level of nitrogen (0.0712 ± 0.0065 and 1.0732 ± 0.0069 day–1) and Superstrain-B variety with the highest nitrogen fertilizer (0.1507 ± 0.0057 and 1.1629 ± 0.0066 day–1), respectively. The results demonstrated that nitrogen fertilizer influenced nearly all the life parameters of the pest which depended on the cultivars. Finally, it could be concluded that Kingston and Superstrain-B were suitable and Earlyurbana and Redston were unsuitable host plant cultivars for H. armigera.
The authors are thankful to the University of Maragheh for partial financial support and the Iranian Research Institute of Plant Protection (Tehran) for providing the facilities and equipment. Also, Mr. Kamyab Farzi, Biorun Company (Karaj) is greatly appreciated for providing H. armigera stock colony.
The authors have declared that no conflict of interests exist.
Akköprü E.P., Atlihan R., Okut H., Chi H. 2015. Demographic assessment of plant cultivar resistance to insect pests: A case study of the dusky-veined walnut aphid (Hemiptera: Callaphididae) on five walnut cultivars. Journal of Economic Entomology 108 (2): 378–387. DOI: 10.1093/jee/tov011.
Amin M.R., Chakma A., Alam M.Z., Hossain M.M., Ge F. 2016. Screening of tomato varieties against tomato fruit borer and associated plant characters. Journal of Agriculture 14 (2): 150–161. DOI: 10.3329/sja.v14i2.31255.
Atlihan R., Kasap I., Ozgokce M.S., Akköprü E.J., Chi H. 2017. Population growth of Dysaphis pyri (Hemiptera: Aphididae) on different pear cultivars with discussion on curve fitting in life-table studies. Journal of Economic Entomology 110 (4): 1890–1898. DOI: 10.1093/jee/tox174.
Awmack C.S., Leather S.R. 2002. Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47: 817–844. DOI: 10.1146/annurev.ento.47.091201.145300.
Bhonwong A., Stout M.J., Attajarusit J., Tantasawat P. 2009. Defensive role of tomato polyphenol oxidases against cotton bollworm (Helicoverpa armigera) and beet armyworm (Spodoptera exigua). Journal of Chemical Ecology 35 (1): 28–38. DOI: 10.1007/s10886-008-9571-7.
Blake A.J., Dosdall L.M., Keddie B.A. 2010. Bottom-up effects of Brassica napus nutrition on the oviposition preference and larval performance of Ceutorhynchus obstrictus (Coleoptera: Curculionidae). Arthropod-Plant Interactions 5 (1): 39–48.
Bosch M., Wright L.P., Gershenzon J., Wasternack C., Hause B., Schaller A., Stintzi A. 2014. Jasmonic acid and its precursor 12-oxophytodienoic acid control different aspects of constitutive and induced herbivore defenses in tomato. Plant Physiology 166: 396–410. DOI: 10.1104/pp.114.237388.
Chau A., Heinz K.M., Davies F.T. 2005. Influences of fertilization on Aphis gossypii and insecticide usage. Journal of Applied Entomology 129 (2): 89–97. DOI: 10.1111/j.1439-0418.2005.00943.x.
Chen Y., Ruberson J.R., Olson D.M. 2008. Nitrogen fertilization rate affects feeding, larval performance, and oviposition preference of the beet army worm, Spodoptera exigua, on cotton. Entomologia Experimentalis and Applicata 126 (3): 244–255. DOI: https://doi.org/10.1111/j.1570....
Chen Y., Olson D.M., Ruberson J.R. 2010. Effects of nitrogen fertilization on tritrophic interactions. Arthropod-Plant Interactions 4 (2): 81–94. DOI: 10.1007/s11829-010-9092-5.
Chi H., Liu H. 1985. Two new methods for the study of insect population ecology. Bulletin of the Institute of Zoology, Academia Sinica 24 (2): 225–240.
Chi H. 1988. Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology 17 (1): 26–34. DOI: https://doi.org/10.1093/ee/17.....
Chi H., Su H.Y. 2006. Age-stage, two-sex life-tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environmental Entomology 35 (1): 10–21. DOI: https://doi.org/10.1603/0046-2....
Chi H. 2016. TWOSEX-MSChart: A computer program for the age-stage, two-sex life-table analysis. Retrieved April 25, 2016. Available on: from
Chu Y.I., Horng S.B. 1994. Effect of slag and nitrogen fertilizer on the damage of Asian corn borer to field corn. Memoirs of the College of Agriculture; National Taiwan University 34 (1): 45–53.
Chuche J., Thiery D. 2012. Egg incubation temperature differently affects female and male hatching dynamics and larval fitness in a leafhopper. Ecology and Evolution 2 (4): 732–739. DOI: 10.1002/ece3.89.
Coqueret V., Le Bot J., Larbat R., Desneux N., Robin C., Adamowicz S. 2017. Nitrogen nutrition of tomato plant alters leaf miner dietary intake dynamics. Journal of Insect Physiology 99: 130–138. DOI: 10.1016/j.jinsphys.
Douglas A.E. 1993. The nutritional quality of phloem sap utilized by natural aphid populations. Ecological Entomology 18 (1): 31–38. DOI.org/10.1111/j.1365-2311.
Downes S., Kriticos D., Parry H., Paull C., Schellhorn N., Zalucki M.P. 2016. A perspective on management of Helicoverpa armigera: Transgenic BT cotton, IPM, and landscapes. Pest Management Science 73: 485–492. DOI: 10.1002/ps.4461.
Efron B., Tibshirani R.J. 1993. An Introduction to the Bootstrap. Chapman and Hall, NewYork, USA.
Fallahnejad-Mojarrad N., Goldasteh Sh., Rafiei-Karahroodi Z., Vafaei Shoushtari R. 2017. Response of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae) to different semi artificial diets. Journal of Agricultural Science and Technology 19: 1303–1318.
Farrokhi M., Gharekhani G.H., Iranipour Sh., Hassanpour M. 2017. Host plant-herbivore-predator interactions in Chrysoperla carnea (Neuroptera: Chrysopidae) and Myzus persicae (Homoptera: Aphididae) on four plant species under laboratory conditions. Journal of Economic Entomology 110 (6): 2342–2350. DOI: 10.1093/jee/tox268.
Fathipour Y., Naseri B. 2011. Soybean cultivars affecting performance of Helicoverpa armigera (Lepidoptera: Noctuidae). p. 599–630. In: “Soybean-Biochemistry, Chemistry and Physiology (T.B. Ng, ed.). In Tech, Rijeka, Croatia. DOI: 10.5772/14838.
Gharekhani G.H., Salek-Ebrahimi H. 2014a. Evaluating the damage of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on some cultivars of tomato under greenhouse condition. Archives of Phytopathology and Plant Protection 47 (4): 429–436. DOI: 10.1080/03235408.2013.811800.
Gharekhani G.H., Salek-Ebrahimi H. 2014b. Life-table parameters of Tuta absoluta (Lepidoptera: Gelechiidae) on different varieties of tomato. Journal of Economic Entomology 107 (5): 1765–1770. DOI: 10.1603/EC14059.
Gillooly J.F., Charnov E.L., West G.B., Savage V.M., Brown J.H. 2002. Effects of size and temperature on developmental time. Nature 417: 70–73. DOI: 10.1038/417070a.
Gomes E.S., Santos V., Avila C.J. 2017. Biology and fertility life-table of Helicoverpa armigera (Lepidoptera: Noctuidae) in different hosts. Entomological Science 20 (1): 419–426. DOI: https://doi.org/10.1111/ens.12....
Goodman D. 1982. Optimal life histories, optimal notation, and the value of reproductive value. The American Naturalist 119 (6): 803–823. DOI: 10.1086/283956.
Grant C.A., Dreksen D.A., Mclaren D.L., Irvine R.B. 2011. Nitrogen fertilizer and urease inhibitor effects on canola seed quality in a one-pass seeding and fertilizing system. Field Crops Research 121 (2): 201–208. DOI: 10.1016/j.fcr.2010.10.012.
Goetz S., Hellwege A., Stenzel I., Kutter C., Hauptmann V., Forner S., McCaig B., Hause G., Miersch O., Wasternack C. 2012. Role of cis-12-oxo-phytodienoic acid in tomato embryo development. Plant Physiology 158: 1715–1727. DOI: 10.1104/pp.111.192658.
Harwood J.F., Chen K., Müller H.G., Wang J.L., Vargas R.I. Carey J.R. 2014. Effects of diet and host access on fecundity and lifespan in two fruit fly species with different life history patterns. Physiological Entomology 38 (1): 81–88. DOI: 10.1111/phen.12006.
Hemati S.A., Naseri B., Ganbalani G.N., Dastjerdi H.R., Golizadeh A. 2012a. Effect of different host plants on nutritional indices of the pod borer, Helicoverpa armigera. Journal of Insect Science 12: 55. DOI: 10.1673/031.012.5501.
Hemming J.D.C., Lindroth R.L. 2003. Effects of light and nutrient availability on aspen: growth, phytochemistry, and insect performance. Journal of Chemical Ecology 28 (7): 1687–1714. DOI: 10.1023/A:1020805420160.
Huang J.S., Nelson P.V., Bailey D.A., Fonteno W.C., Mingis N.C. 2002. Assessment of the need for nitrogen, phosphorus, potassium, and sulfur preplant nutrients for plug seedling growth. Hort Science 37 (3): 529–533. DOI: 10.21273/HORTSCI.37.3.529.
Huang Y.B., Chi H. 2013. Life-tables of Bactrocera cucurbitae (Diptera: Tephritidae): with an invalidation of the jackknife technique. Journal of Applied Entomology137 (5): 327–339. DOI: 10.1038/npre.2012.7070.1.
Hwang S.Y., Liu C.H., Shen T.C. 2008. Effects of plant nutrient availability and host plant species on the performance of two Pieris butterflies (Lepidoptera: Pieridae). Biochemical Systematics and Ecology 36 (7): 505–513. DOI: 10.1016/j.bse.2008.03.001.
Jaleel W., Yin J., Wang D., He Y., Lu L., Shi H. 2017. Using two-sex life tables to determine fitness parameters of four Bactroceraspecies (Diptera: Tephritidae) reared on a semi-artificial diet. Bulletin of Entomological Research 108 (6): 707–714. DOI: https://doi.org/10.1017/s00074....
Jallow M.F.A., Matsumura M. 2001. Influence of temperature on the rate of development of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). Applied Entomology and Zoology 36 (4): 427–430. DOI: 10.1303/aez.2001.427.
Jallow M.F.A., Cunningham J.P., Zalucki M.P. 2004. Intra-specific variation for host plant use in Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae): implications for management. Crop Protection 23 (10): 955–964. DOI: 10.1016/j.cropro.2004.02.008.
Jha R.K., Chi H., Tang L.C. 2012. A comparison of artificial diet and hybrid sweet corn for the rearing of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) based on life-table characteristics. Environmental Entomology 41 (1): 30–39. DOI: 10.1603/EN11206.
Jha R.K., Tuan S.J., Chi H., Tang L.C. 2014. Life-table and consumption capacity of corn earworm, Helicoverpa armigera, fed asparagus, Asparagus officinalis. Journal of Insect Science 14: 34. DOI: 10.1093/jis/14.1.34.
Kim D.S., Lee J.H. 2002. Egg and larval survivorship of Carposina sasakii (Lepidoptera: Carposinidae) in apple and peach and their effects on adult population dynamics in orchards. Environmental Entomology 31 (4): 686–692. DOI: https://doi.org/10.1603/0046-2....
Konishi M., Yanagisawa S. 2013. An NLP-binding site in the 3’ flanking region of the nitrate reductase gene confers nitrate-inducible expression in Arabidopsis. Journal of Soil Science Plant Nutrition 59: 612–620. DOI: 10.1080/00380768.2013.809602.
Kouhi D., Naseri B., Golizadeh A. 2014. Nutritional performance of the tomato fruit borer, Helicoverpa armigera, on different tomato cultivars. Journal of Insect Science 14: 102. DOI: 10.1673/031.014.102.
Kulkarni U.S. 2004. Comparative studies on the biology of Helicoverpa armigera on different food substrates. Journal of Soils and Crops 14: 207–208.
Larbat R., Le Bot J., Bourgaud F., Robin C., Adamowicz S. 2012. Organ‐specific responses of tomato growth and phenolic metabolism to nitrate limitation. Plant Biology 14 (5): 760–769. DOI: 10.1111/j.1438-8677.2012.00564.x.
Liu Z.D., Li D.M., Gong P.Y., Wu K.J. 2004. Life-table studies of the cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae), on different host plants. Environmental Entomology 33 (6): 1570–1576. DOI: https://doi.org/10.1603/0046-2....
Liu J.P., Huang W.K., Chi H., Wang C.H., Hua H.X., Wu G. 2017. Effects of elevated CO2 on the fitness and potential population damage of Helicoverpa armigera based on two-sex life table. Scientific Reports 7: 1119. DOI: 10.1038/s41598-017-01257-7.
Lukefahr M.J., Houghtaling J.E., Graham H.M. 1971. Supression of Heliothis population with glabrous cotton stains. Journal of Economic Entomology 64: 486–488.
Mahmudunnabi M., Dutta N.K., Rahman A.K.M.Z., Alam S.N. 2013. Development of biorational-based integrated pest management package against pod borer, Helicoverpa armigera Hubner infesting chickpea. Journal of Biopesticides 6 (2): 108–111.
Maino J.L., Pirtle E.I., Kearney M.R. 2017. The effect of egg size on hatch time and metabolic rate: theoretical and empirical insights on developing insect embryos. Functional Ecology 31 (1): 227–234. DOI: 10.1111/1365-2435.12702.
Meyer J.S., Ingersoll C.G., McDonald L.L., Boyce M.S. 1986. Estimating uncertainty in population growth rate: Jackknife vs. bootstrap techniques. Ecological Society of America 67 (5): 1156–1166.
Mooney K.A., Pratt R.T., Singer M.S. 2012. The tri-trophic interactions hypothesis: interactive effects of host plant quality, diet breadth and natural enemies on herbivores. Plos One 7 (4): e 34403. https://doi.org/10.1371/journa....
Moreira X., Abdala-Roberts L., Gols R., Francisco M. 2018. Plant domestication decreases both constitutive and induced chemical defences by direct selection against defensive traits. Scientific Reports 8 (1): 12678. DOI: 10.1038s41598-018-310410.
Muthukumaran N. 2016. Biophysical and biochemical factors of resistance in tomato accessions as influenced by selected bio inoculants against fruit worm Helicoverpa armigera (Hubner). Journal of Current Microbiology and Applied Sciences 5 (1): 252–262. DOI.org/10.20546/ijcmas.2016.5....
Naseri B., Golparvar Z., Razmjou J., Golizadeh A. 2014. Agestage, two-sex life-table of Helicoverpa armigera (Lepidoptera: Noctuidae) on different bean cultivars. Journal of Agricultural Science and Technology 16 (1): 19–32.
Peterson J.A., Ode P.J., Oliveira-Hofman C., Harwood J.D. 2016. Integration of plant defense traits with biological control of arthropod pests: challenges and opportunities. Fronties in Plant Science 7: 1794. DOI: 10.3389/fpls.2016.01794.
Price P.W., Bouton C.E., Gross P., McPheron B.A., Thompson J.N., Weis A.E. 1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 11: 41–65.
Prudic K.L., Oliver J.C., Bowers M.D. 2005. Soil nutrient effects on oviposition preference, larval performance and chemical defense of a specialist insect herbivore. Oecologia 143 (4): 578–587. DOI: 10.1007/s00442-005-0008-5.
Razmjou J., Moahrramipour S., Fathipour Y., Mirhoseini S.Z. 2006. Effect of cotton cultivar on performance of Aphis gossypii (Homoptera: Aphididae) in Iran. Journal of Economic Entomology 99 (5): 1820–1825. DOI: 10.1603/0022-0493-99.5.1820.
Razmjou J., Naseri B., Hemati S.A. 2014. Comparative performance of the cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) on various host plants. Journal of Pest Science 87 (1): 29–37. DOI: 10.1007/s10340-013-0515-9.
Reddy G.V.P., Chi H. 2015. Demographic comparison of sweet potato weevil reared on a major host, Ipomoea batatas, and an alternative host. International Journal of Scientific Reports 5: 11871. DOI: 10.1038/srep11871.
Safuraie P.S., Fathipour Y., Talebi A.A. 2014. Evaluation of tomato cultivars to Helicoverpa armigera using two-sex life table parameters in laboratory. Journal of Asia-Pacific Entomology 17: 837–844. DOI: 10.1016/j.aspen.2014.08.004.
Sajjad M., Ashfaq M., Suhail A., Akhtar Sh. 2011. Screening of tomato genotypes for resistance to tomato fruit borer, elicoverpa armigera in Pakistan. Journal of Agricultural Sciences 48 (1): 49–52.
Setiawati W. 1990. The effects of sublethal concentration of several insecticides on fecundity and longevity of Crocidolomia binotalis (Zell.). Bulletin of Penel Horticulture 20: 19–25.
Sharma L.K., Bali S.K. 2017. A review of methods to improve nitrogen use efficiency in agriculture Journal of Sustainability 10 (2): 51. DOI: https://doi.org/10.3390/su1001....
Smith C.M. 2005. Plant Resistance to Arthropods – Molecular and Conventional Approaches. Springer Verlag, Dordrecht, the Netherlands, 423 pp.
Suzana C.S., Damiani R., Fortuna L.S., Salvadori J.R. 2015. Performance of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) larvae in different food sources. Pesquisa Agropecuaria Trop 45 (4): 480–485. DOI.org/10.1590/1983-40632015v....
Talekar N.S., Opena R.T., Hanson P. 2006. Helicoverpa armigera management: A review of AVRDC’s research on host plant resistance in tomato. Crop Protection 25 (5): 461–467. DOI: https://doi.org/10.1016/j.crop....
Tan C.W., Chiang S.Y., Ravuiwasa K.T., Yadav J., Hwang S.Y. 2012. Jasmonate-induced defenses in tomato against Helicoverpa armigera depend in part on nutrient availability, but artificial induction via methyl jasmonate does not. Arthropod-Plant Interactions 6 (4): 531–541. DOI: 10.1007/s11829-012-9206-3.
Teakle R.E. 1991. Laboratory culture of Heliothis species and identification of disease. p. 22–29. In: “Heliothis: Research Methods and Prospects” (M.P. Zalucki, ed.). Springer Verlag New York Inc.
Throop H.L., Lerdau M.T. 2004. Effects of nitrogen deposition on insect herbivory: implications for community and ecosystem processes. Ecosystems 7 (2): 109–133.
Trdan S., Znidarcic D., Kac M., Vidrih M. 2008. Yield of early white cabbage grown under mulch and non-mulch conditions with low populations of onion Thrips (Thrips tabaci Lindeman). International Journal of Pest Management 54 (4): 309–318. DOI: https://doi.org/10.1080/096708....
Truzi C.C., Fernanda Vieira N., Lucas de Laurentis V., Vacari A.M., Bortoli S.A.D. 2017. Development and feeding behavior of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) on different sunflower genotypes under laboratory conditions. Arthropod-Plant Interactions 11 (6): 797–805. DOI: 10.1007/s11829-017-9534-4.
Tsai J.H., Wang J. 2001. Effects of host plants on biology and lifetable parameters of Aphid spiraecola (Homoptera: Aphididae). Environmental Entomology 30 (1): 45–50. DOI: https://doi.org/10.1603/0046-2....
Tuan S. J., Yeh C.C., Atlihan R., Chi H. 2016. Linking life table and predation rate for biological control: A comparative study of Eocanthecona furcellata (Hemiptera: Pentatomidae) fed on Spodoptera litura (Lepidoptera: Noctuidae) and Plutella xylostella (Lepidoptera: Plutellidae). Journal of Economic Entomology 109: 13–24. DOI: 10.1093/jee/tov265.
Veromann E., Toome M., Kannaste A., Kaasik R., Copolovici L., Flink J. 2013. Effects of nitrogen fertilization on insect pests, their parasitoids, plant diseases and volatile organic compounds in Brassica napus. Crop Protection 43: 79–88. DOI: https://doi.org/10.1016/j.crop....
Wang L.Z.L., Li Ch.R., Yuan J.J., Li S.X., Wang X.P., Chi H. 2017. Demographic comparison of Henosepilachna vigintioctopunctata (F.) (Coleoptera: Coccinellidae) reared on three cultivars of Solanum melongena L. and a wild hostplant Solanum nigrum. Journal of Economic Entomology 110 (5): 2084–2091. DOI: 10.1093/jee/tox207.
Yu-Tzu H., Tse-Chi Sh., Shaw-Yhi H. 2009. Soil fertility management and pest responses: A comparison of organic and synthetic fertilization. Journal of Economic Entomology 102 (1): 160–169. DOI: https://doi.org/10.1603/029.10....
Zehnder C., Huntr M. 2008. Effects of nitrogen deposition onthe interaction between an aphid and its host plant. Journal of Ecological Entomology 33 (1): 24. DOI: https://doi.org/10.1111/j.1365....