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Development, survivorship and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) under fluctuating temperatures

Published online by Cambridge University Press:  11 September 2014

George K. Mironidis
George K. Mironidis*
Affiliation:
Institute of Molecular Biology and Biotechnology, FORTH, 70013 Heraklion, Greece Laboratory of Molecular Entomology, Department of Biology, University of Crete, 71409 Heraklion, Greece
*
*Author for correspondence Phone: +302374023245 Fax: +302374023245 E-mail: geomironidis@gmail.com
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Abstract

Laboratory studies were conducted to assess the effect of temperature on the survival, development, longevity and fecundity of Helicoverpa armigera (Lepidoptera: Noctuidae) at eight different fluctuating temperatures with an amplitude ±9 °C under constant photoperiodic conditions of 16:8 h (L:D). H. armigera achieved complete development from egg to adult emergence between mean 17.5 and 32.5 °C. At mean 35 °C, all newly hatched larvae died and at mean 15 °C entered diapause at pupal stage. The lower developmental thresholds of the immature stages were estimated by a linear model and ranged from 4.63 °C (pupal stage) to 7.69 °C (egg stage). The developmental thresholds estimated by a nonlinear model were slightly higher than those estimated by the linear model. Adult longevity and fecundity were reduced at mean fluctuating temperatures 17.5 and 32.5 °C, but tended to be independent of the pattern of temperature change at moderate temperatures. The maximum reproductive performance, 1130 eggs per female, was observed at mean 25 °C. The intrinsic rates of increase were positive, meaning that H. armigera could be expected to persist or increase in number between mean 17.5 and 32.5 °C, with the maximum value at mean 27.5 °C. H. armigera survives, develops and reproduces within a wide range of fluctuating temperatures, while it completes the above functions with different levels of success at different mean temperatures of diurnal variation. Comparison of our results with similar data from the literature involving constant conditions is discussed. This information will provide a better understanding of H. armigera phenology and population dynamics under natural conditions and is essential to understanding the ecological and evolutionary consequences of climate change on this important species.

Keywords

Helicoverpa armigerafluctuating temperaturesdevelopmental timesurvivallife tables
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 104 , Issue 6 , December 2014 , pp. 751 - 764
Copyright
Copyright © Cambridge University Press 2014 

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References

Allsopp, P.G., Daglish, G.J., Taylor, M.F.J. & Gregg, P.C. (1991) Measuring development of Heliothis species. pp. 90–101 in Zalucki, M.P. (Ed.) Heliothis: Research Methods and Prospects. New York, USA, Springer – Verlag.Google Scholar
Andrewartha, H.G. (1970) Introduction to the Study of Animal Populations. Chicago, IL, University of Chicago Press.Google Scholar
Bale, J.S. & Hayward, S.A.L. (2010) Insect overwintering in a changing climate. The Journal of Experimental Biology 213, 980–994.CrossRefGoogle Scholar
Bartekova, A. & Praslicka, J. (2006) The effect of ambient temperature on the development of cotton bollworm (Helicoverpa armigera Hübner, 1808). Plant Protection Science 42, 135–138.Google Scholar
Beck, S.D. (1980) Insect Photoperiodism. 2nd edn. New York, USA, Academic Press.Google Scholar
Beck, S.D. (1983 a) Insect thermoperiodism. Annual Review of Entomology 28, 91–108.Google Scholar
Beck, S.D. (1983 b) Thermal and thermoperiodic effects on larval development and diapause in the European corn borer, Ostrinia nubilalis . Journal of Insect Physiology 29, 107–112.CrossRefGoogle Scholar
Beck, S.D. (1991) Thermoperiodism. pp. 199–228 in Lee, R.E. Jr. & Denlinger, D.L. (Eds) Insects at Low Temperature. New York, London, Chapman and Hall.Google Scholar
Behrens, W., Hoffmann, K.H., Kempa, S., Gäbler, S. & Merkel-Wallner, G. (1983) Effects of diurnal thermoperiods and quickly oscillating temperatures on the development and reproduction of crickets, Gryllus bimacullatus . Oecologia 59, 279–287.Google Scholar
Brakefield, P.M. & Mazzotta, V. (1995) Matching field and laboratory environments: effects of neglecting daily temperature variation on insect reaction norms. Journal of Evolutionary Biology 8, 559–573.Google Scholar
Bryant, R.S., Bale, J.S. & Thomas, D. (1999) Comparison of development and growth of nettle-fedding larvae of Nymphalidae (Lepidoptera) under constant and alternating temperature regimes. European Journal of Entomology 96, 143–148.Google Scholar
Bursell, E. (1964) Environmental aspects: temperature. pp. 283–317 in Rockstein, M. (Ed.) The Physiology of Insects, Vol. I. New York, London, Academic Press.Google Scholar
Carey, J.R. (1993) Applied Demography for Biologists with Special Emphasis on Insects. New York, Oxford University Press.Google Scholar
Carrington, L.B., Armijos, M.V., Lambrechts, L., Barker, C.M. & Scott, T.W. (2013) Effects of fluctuating daily temperatures at critical thermal extremes on Aedes aegypti life-history traits. PLoS ONE 8, e58824.Google Scholar
Cloudsley-Thompson, J.L. (1953) The significance of fluctuating temperatures on the physiology and ecology of insects. Entomologist 86, 183–189.Google Scholar
Davis, I.A., Radcliffe, E.B. & Ragsdale, D.W. (2006) Effects of high and fluctuating temperatures on Myzus persicae (Hemiptera: Aphididae). Environmental Entomology 35, 1461–1468.Google Scholar
Dhileepan, K., Trevino, M. & Raghu, S. (2005) Effects of temperature on the survival of Aconophora compressa Walker (Hemiptera: Membracidae): implications for weed biocontrol. Australian journal of Entomology 44, 457–462.Google Scholar
Easterling, D.R., Meehl, G.A., Parmesan, C., Changnon, S.A., Karl, T.R. & Mearns, L.O. (2000) Climate extremes: observations, modelling, and impacts. Science 289, 2068–2074.Google Scholar
Eubank, W.P., Atmar, J.W. & Ellington, J.J. (1973) The significance and thermodynamics of fluctuating versus static thermal environments on Heliothis zea egg development rates. Environmental Entomology 2, 491–496.Google Scholar
Fantinou, A.A., Perdikis, D.Ch. & Chatzoglou, C.S. (2003) Development of immature stages of Sesamia nonagrioides (Lepidoptera: Noctuidae) under alternating and constant temperatures. Environmental Entomology 32, 1337–1342.Google Scholar
Fathipour, Y. & Sedaratian, A. (2013) Integrated Management of Helicoverpa armigera in Soybean Cropping Systems, Soybean – Pest Resistance, Prof. Hany El-Shemy (Ed.), ISBN: 978-953-51-0978-5, InTech, doi: 10.5772/54522. Available online at http://www.intechopen.com/books/soybean-pest-resistance/integrated-management-of-helicoverpa-armigera-in-soybean-cropping-systems Google Scholar
Fields, P.A. (2001) Protein function at thermal extremes: balancing stability and flexibility. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 129, 417–431.Google Scholar
Fischer, K., Kölzow, N., Höltje, H. & Karl, I. (2011) Assay conditions in laboratory experiments: is the use of constant rather than fluctuating temperatures justified when investigating temperature-induced plasticity? Oecologia 166, 23–33.Google Scholar
Fitt, G.P. (1989) The ecology of heliothis in relation to agroecosystems. Annual Review of Entomology 34, 17–52.Google Scholar
Foley, D.H. (1981) Pupal development rate of Heliothis armigera (Hübner) (Lepidoptera: Noctuidae) under constant and fluctuating temperatures. Journal of the Australian Entomological Society 20, 13–20.Google Scholar
Gillott, C. (2005) Entomology. 3rd edn. Dordrecht, Netherlands, Springer.Google Scholar
Grimaldi, D. & Engel, M.S. (2005) Evolution of the Insects. New York, Cambridge University Press.Google Scholar
Gutierrez, A.P. (1996) Applied Population Ecology: a Supply-Demand Approach. pp. 42–53. New York, John Wiley & Sons, Inc.Google Scholar
Hagstrum, D.W. & Hagstrum, W.R. (1970) A simple device for producing fluctuating temperatures, with an evaluation of the ecological significance of fluctuating temperatures. Annals of the Entomological Society of America 63, 1385–1389.Google Scholar
Hagstrum, D.W. & Leach, C.E. (1973) Role of constant and fluctuating temperature in determining development time and fecundity of three species of stored-products Coleoptera. Annals of the Entomological Society of America 66, 407–419.Google Scholar
Hagstrum, D.W. & Milliken, G.A. (1991) Modeling differences in insect developmental times between constant and fluctuating temperatures. Annals of the Entomological Society of America 84, 369–379.Google Scholar
Hardwick, D.F. (1965) The corn earworm complex. Memoirs of the American Entomological Society 40, 1–247.Google Scholar
Hoffmann, K.H. (1980) Anpassungen im Stoffwechsel von Insekten an tagesperiodische Wechseltemperaturen. Verhandlungen der Deutschen Zoologischen Gesellschaft 1980, 214–227.Google Scholar
Hogg, D.B. (1985) Potato leafhopper (Homoptera: Cicadellidae) immature development, life tables, and population dynamics under fluctuating temperature regimes. Environmental Entomology 14, 349–355.Google Scholar
Howe, R.W. (1967) Temperature effects on embryonic development in insects. Annual Review of Entomology 12, 15–42.CrossRefGoogle ScholarPubMed
Huey, R.B. & Kingsolver, J.G. (1989) Evolution of thermal sensitivity of ectotherm performance. Trends in Ecology & Evolution 4, 131–132.Google Scholar
Humpesch, U.H. (1980) Effect of temperature on the hatching time of eggs of five Ecdyonurus spp. (Ephemeroptera) from Austrian streams and English streams, rivers and lakes. Journal of Animal Ecology 49, 317–333.Google Scholar
Humpesch, U.H. (1982) Effect of fluctuating temperature on the duration of embryonic development in two Ecdyonurus spp.and Rhithrogena cf. hybrida (Ephemeroptera) from Austrian streams. Oecologia (Berlin) 55, 285–288.Google Scholar
Jallow, M.F.A. & Matsumura, M. (2001) Influence of temperature on the rate of development of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Applied Entomology and Zoology 36, 427–430.Google Scholar
Johansson, F., Stoks, R., Rowe, L. & De Block, M. (2001) Life history plasticity in a damselfly: effects of combined time and biotic constraints. Ecology 82, 1857–1869.Google Scholar
Kaufmann, O. (1932) Einige Bemerkungen über den Einfluß von Temperaturschwankungen auf die Entwicklungsdauer und Streuung bei Insekten und seine graphische Darstellung durch Ketten-linie und Hyperbel. Zeitschrift für Morphologie und Ökologie der Tiere 25, 354–361.Google Scholar
Kay, I.R. (1981) The effect of constant temperatures on the development time of eggs of Heliothis armigera (Hübner) (Lepidoptera: Noctuidae). Journal of the Australian Entomological Society 20, 155–156.Google Scholar
Keen, R. (1979) Effects of fluctuating temperature on duration of egg development of Chydorus sphaerieus (Cladocera, Crustacea). Journal of Thermal Biology 4, 5–8.Google Scholar
Kieckhefer, R.W. & Elliott, N.C. (1989) Effect of fluctuating temperatures on development of immature Russian wheat aphids (Homoptera: Aphididae) and demographic statistics. Journal of Economic Entomology 82, 119–122.Google Scholar
Kingsolver, J.G., Ragland, G.J. & Diamond, S.E. (2009) Evolution in a constant environment: thermal fluctuations and thermal sensitivity of laboratory and field populations of Manduca sexta . Evolution 63, 537–541.Google Scholar
Kingsolver, J.G., Woods, H.A., Buckley, L.B., Potter, K.A., MacLean, H.J. & Higgins, J.K. (2011) Complex life cycles and the responses of insects to climate change. Integrative and Comparative Biology 51, 719–732.Google Scholar
Lactin, D.J., Holliday, N.J., Johnson, D.L. & Craigen, R. (1995) Improved rate model of temperature-dependent development by arthropods. Environmental Entomology 24, 68–75.Google Scholar
Lamb, K.P. (1961) Some effects of fluctuating temperatures on metabolism, development, and rate of population growth in the cabbage aphid, Brevecoryne brassicae . Ecology 42, 740–745.Google Scholar
Lamb, R.J. & Gerber, G.H. (1985) Effects of temperature on the development, growth, and survival of larvae and pupae of a north – temperate chrysomelid beetle. Oecologia (Berlin) 67, 8–18.Google Scholar
Liu, S.S., Zhang, G.M. & Zhu, J. (1995) Influence of temperature variations on the rate of development in insects: analysis of case studies from entomological literature. Annals of the Entomological Society of America 88, 107–119.Google Scholar
Liu, S.S., Chen, F.Z. & Zalucki, M.P. (2002) Development and survival of the Diamondback Moth (Lepidoptera: Plutellidae) at constant and alternating temperatures. Environmental Entomology 31, 221–231.Google Scholar
Liu, Z., Li, D., Gong, P. & Wu, K. (2004) Life table studies of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), on different host plants. Environmental Entomology 33, 1570–1576.Google Scholar
Logan, J.A., Wollkind, D.J., Hoyt, S.C. & Tanigoshi, L.K. (1976) An analytic model for description of temperature dependent rate phenomena in arthropods. Environmental Entomology 5, 1133–1140.Google Scholar
Maharaj, R. (2003) Life table characteristics of Anopheles arabiensis (Diptera: Culicidae) under simulated seasonal conditions. Journal of Medical Entomology 40, 737–742.Google Scholar
Messenger, P.S. (1964) The influence of rhythmically fluctuating temperatures on the development and reproduction of the spotted alfalfa aphid, Therioaphis maculata . Journal of Economic Entomology 57, 71–79.Google Scholar
Mironidis, G.K. (2009) Study of bio-ecology of Helicoverpa armigera (Lepidoptera: Noctuidae) and its parasitoid Hyposoter didymator (Hymenoptera: Ichneumonidae) in northern Greece. PhD Thesis, Aristotle University of Thessaloniki, Greece.Google Scholar
Mironidis, G.K. & Savopoulou-Soultani, M. (2008) Development, survivorship, and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) under constant and alternating temperatures. Environmental Entomology 37, 16–28.Google Scholar
Mironidis, G.K. & Savopoulou-Soultani, M. (2010) Effects of heat shock on survival and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) adults. Journal of Thermal Biology 35, 59–69.CrossRefGoogle ScholarPubMed
Mironidis, G.K. & Savopoulou-Soultani, M. (2012) Effects of thermophotoperiod on growth parameters of Helicoverpa armigera . Entomologia Experimentalis et Applicata 142, 60–70.Google Scholar
Mironidis, G.K., Stamopoulos, D.C. & Savopoulou-Soultani, M. (2010) Overwintering survival and spring emergence of Helicoverpa armigera (Lepidoptera: Noctuidae) in Northern Greece. Environmental Entomology 39, 1068–1084.Google Scholar
Paaijmans, K.P., Heinig, R.L., Seliga, R.A., Blanford, J.I., Blanford, S., Murdock, C.C. & Thomas, M.B. (2013) Temperature variation makes ectotherms more sensitive to climate change. Global Change Biology 19, 2373–2380.Google Scholar
Petavy, G., David, J.R., Gibert, P. & Moreteau, B. (2001) Viability and rate of development at different temperatures in Drosophila: a comparison of constant and alternating thermal regimes. Journal of Thermal Biology 26, 29–39.Google Scholar
Price, P.W. (1997) Insect Ecology. pp. 315–325. 3rd edn. New York, John Wiley & Sons, Inc.Google Scholar
Qureshi, M.H., Murai, T., Yoshida, H., Shiraga, T. & Tsumuki, H. (1999) Effects of photoperiod and temperature on development and diapause induction in the Okayama population of Helicoverpa armigera (Hb.) (Lepidoptera: Noctuidae). Applied Entomology and Zoology 34, 327–331.Google Scholar
Ratte, H.P. (1985) Temperature and insect development. pp. 36–66 in Hoffman, K. (Ed.) Environmental Physiology and Biochemistry of Insects. New York, Springer.Google Scholar
Richards, A.G. & Suanraksa, S. (1962) Energy expenditure during embryonic development under constant and variable temperatures [Oncopellus fasciatus (Dallas)]. Entomologia Experimentalis et Applicata 5, 167–178.Google Scholar
Rock, C.G. (1985) Thermal and thermoperiodic effects on larval and pupal development and survival in tufted apple bud moth (Lepidoptera: Tortricidae). Environmental Entomology 14, 637–640.Google Scholar
Roltsch, W.J., Mayse, M.A. & Clausen, K. (1990) Temperature – dependent development under constant and fluctuating temperature: comparison of linear versus nonlinear methods for modelling development of western grapeleaf skeletonizer (Lepidoptera: Zygaenidae). Environmental Entomology 19, 1689–1697.Google Scholar
Saffar, Z.Y.A., Grainger, J.N.R. & Aldrich, J. (1996) Temperature and humidity affecting development, survival and weight loss of the pupal stage of Drosophila melanogaster, and the influence of alternating temperature on the larvae. Journal of Thermal Biology 21, 389–396.Google Scholar
Sharpe, P.J.H. & DeMichele, D.W. (1977) Reaction kenetics of poikilotherm development. Journal of Thermal Biology 64, 649–670.Google Scholar
Singh, A.K. & Lakhotia, S.C. (2000) Tissue-specific variations in the induction of Hsp70 and Hsp64 by heat shock in insects. Cell Stress and Chaperones 5, 90–97.Google Scholar
Sokal, R.R. & Rohlf, F.J. (1995) Biometry. 3rd edn. New York, USA, Freeman.Google Scholar
SPSS Inc. (2006) SPSS 14 for Windows, User's Guide. Chicago, IL, USA, SPSS, Inc.Google Scholar
Stamopoulos, D.C. (1989) Effects of photoperiod on the biology of Acanthoscelides obtectus Say. Journal of Applied Entomology 107, 150–154.Google Scholar
StatSoft Inc. (2001) STATISTICA for Windows (Data Analysis Software System), Version 6. Tulsa, USA, StatSoft, Inc.Google Scholar
Tauber, M.J., Tauber, C.A. & Masaki, S. (1986) Seasonal Adaptations of Insects. New York, USA, Oxford University Press.Google Scholar
Twine, P.H. (1978) Effect of temperature on the development of larvae and pupae of corn earworm, Heliothis armigera (Hübner) (Lepidoptera: Noctuidae). Queensland Journal of Agricultural & Animal Sciences 35, 23–28.Google Scholar
Vangansbeke, D., De Schrijver, L., Spranghers, T., Audenaert, J., Verhoeven, R., Nguyen, D.T., Gobin, B., Tirry, L. & De Clercq, P. (2013) Alternating temperatures affect life table parameters of Phytoseiulus persimilis, Neoseiulus californicus (Acari: Phytoseiidae) and their prey Tetranychus urticae (Acari: Tetranychidae). Experimental and Applied Acarology 61, 285–298.Google Scholar
Vargas, R.I., Walsh, W.A., Kanehisa, D., Stark, J.D. & Nishida, T. (2000) Comparative demography of three Hawaiian fruit flies (Diptera: Tephritidae) at alternating temperatures. Annals of the Entomological Society of America 93, 75–81.Google Scholar
Vose, R.S., Easterling, D.R. & Gleason, B. (2005) Maximum and minimum temperature trends for the globe: an update through 2004. Geophysical Research Letters 32, L23822.Google Scholar
Welbers, P. (1975) The influence of diurnally alternating temperature on the pink bollworm, Pectinophora I. Duration of development, larval body weight and fecundity. Oecologia (Berl.) 21, 31–42.Google Scholar
Wilson, A.G.L., Lewis, T. & Cunningham, R.B. (1979) Overwintering and emergence of Heliothis armigera (Hubner) (Lepidoptera: Noctuidae) in Namoi Valley, New South Wales. Bulletin of Entomological Research 69, 97–109.Google Scholar
Worner, S.P. (1992) Performance of phonological models under variable temperature regimes: consequences of the Kaufmann or rate summation effect. Environmental Entomology 21, 689–699.Google Scholar
Yeargan, K.V. (1980) Effects of temperature on development rate of Telenomus podisi (Hymenoptera: Scelionidae). Annals of the Entomological Society of America 73, 339–342.Google Scholar
Zalucki, M.P., Daglish, G., Firempong, S. & Twine, P.H. (1986) The biology and ecology of Heliothis armigera (Hubner) and H. punctigera Wallengren (Lepidoptera: Noctuidae) in Australia: what do we Know? Australian Journal of Zoology 34, 779–814.Google Scholar
Zalucki, M.P., Murray, D.A.H., Gregg, P.C., Fitt, G.P., Twine, P.H. & Jones, C. (1994) Ecology of Helicoverpa armigera (Hübner) and H. punctigera (Wallengren) in the inland of Australia: larval sampling and host plant relationships during winter and spring. Australian Journal of Zoology 42, 329–346.Google Scholar