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Effects of constant and changing temperature conditions on diapause induction in Helicoverpa armigera (Lepidoptera: Noctuidae)

Published online by Cambridge University Press:  06 September 2011

G.K. Mironidis  and
M. Savopoulou-Soultani
G.K. Mironidis*
Affiliation:
Aristotle University of Thessaloniki, Faculty of Agriculture, Department of Plant Protection, Laboratory of Applied Zoology and Parasitology, 54124 Thessaloniki, Greece
M. Savopoulou-Soultani
Affiliation:
Aristotle University of Thessaloniki, Faculty of Agriculture, Department of Plant Protection, Laboratory of Applied Zoology and Parasitology, 54124 Thessaloniki, Greece
*
*Author for correspondence Fax: +302310998832 E-mail: [email protected], [email protected]
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Abstract

The effects of photoperiod and temperature on the induction and termination of facultative pupal diapause in Helicoverpa armigera (Lepidoptera: Noctuidae) were investigated under laboratory conditions. Exposing H. armigera larvae to both constant and fluctuating temperature regimes with a mean of 25°C and 20°C resulted in a type-III photoperiodic response curve of a short-long day insect. The long-day critical daylengths for diapause induction were ten hours and 12 hours at the constant temperatures of 25°C and 20°C, respectively. Higher incidences of diapause and higher values both for the longer and the shorter critical photoperiods for diapause induction were observed at fluctuating regimes compared with the corresponding constant ones. At alternating temperatures, the incidence of diapause ranged from 4.2% to 33.3% and was determined by the temperature amplitude of the thermoperiod and by the interaction of cryophase or thermophase with the photoperiod. Helicoverpa armigera larvae seem to respond to photoperiodic stimuli at temperatures >15°C and <30°C; all insects entered diapause at a constant temperature of 15°C, whereas none did so at a constant temperature of 30°C under all the photoperiodic regimes examined. Although chilling was not a prerequisite for diapause termination, exposure of diapausing pupae to chilling conditions significantly accelerated diapause development and the time of adult emergence. Therefore, temperature may be the primary factor controlling the termination of diapause in H. armigera.

Keywords

Helicoverpa armigeradiapause incidencephotoperiodtemperature
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 2 , April 2012 , pp. 139 - 147
Copyright
Copyright © Cambridge University Press 2011

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References

Beck, S.D. (1980) Insect Photoperiodism. 2nd end.New York, USA, Academic Press.Google Scholar
Beck, S.D. (1983a) Insect thermoperiodism. Annual Review of Entomology 28, 91–108.CrossRefGoogle Scholar
Beck, S.D. (1983b) 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. (1985) Effects of thermoperiod on photoperiodic determination of diapause in Ostrinia nubilalis. Journal of Insect Physiology 31, 41–46.CrossRefGoogle Scholar
Beck, S.D. (1988) Thermoperiod and larval development of Agrotis ipsilon (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 81, 831–835.CrossRefGoogle Scholar
Bradshaw, W.E. (1980) Thermoperiodism and the thermal environment of the pitcher-plant mosquito, Wyeomyia smithii. Oecologia 46, 13–17.CrossRefGoogle ScholarPubMed
Brown, J.R. & Phillips, J.R. (1991) Thermoperiod effects on diapause induction in Microplitis croceipes (Cresson) (Hymenoptera: Braconidae). Environmental Entomology 20, 1444–1446.CrossRefGoogle Scholar
Browning, T.O. (1979) Timing of the action of photoperiod and temperature on events leading to diapause and development in pupae of Heliothis punctigera (Lepidoptera: Noctuidae). Journal of Experimental Biology 83, 261–269.CrossRefGoogle Scholar
Chippendale, G.M., Reddy, A.S. & Catt, C.L. (1976) Photoperiodic and thermoperiodic interaction in the regulation of the larval diapause of Diatraea grandiosella. Journal of Insect Physiology 22, 823–828.CrossRefGoogle Scholar
Cloudsley-Thompson, J.L. (1953) The significance of fluctuating temperatures on the physiology and ecology of insects. Entomologist 86, 183–189.Google Scholar
Coaker, T.H. (1959) Investigations on Heliothis armigera in Uganda. Bulletin of Entomological Research 50, 487–506.CrossRefGoogle Scholar
Cullen, J.M. & Browning, T.O. (1978) The influence of photoperiod and temperature on the induction of diapause in pupae of Heliothis punctigera. Journal of Insect Physiology 24, 595–601.CrossRefGoogle Scholar
Danks, H.V. (1987) Insect Dormancy: An Ecological Perspective. Ottawa, Canada, Biological Survey of Canada.Google Scholar
Danilevsky, A.S. (1961) Photoperiodism and Seasonal Development of Insects. Edinburgh, Scotland, UK, Oliver and Boyd (1965, English translation).Google Scholar
Eizaguirre, M., Lopez, C., Asin, L. & Albajes, R. (1994) Thermoperiodism, photoperiodism and sensitive stage in the diapause induction of Sesamia nonagrioides (Lepidoptera: Noctuidae). Journal of Insect Physiology 40, 113–119.CrossRefGoogle Scholar
Fantinou, A.A. & Chourdas, M.Th. (2006) Thermoperiodic effects on larval growth parameters of the Sesamia nonagrioides (Lepidoptera: Noctuidae). Journal of Pest Science 79, 43–49.CrossRefGoogle Scholar
Fantinou, A.A. & Kagkou, E.A. (2000) Effect of thermoperiod on diapause induction of Sesamia nonagrioides (Lepidoptera, Noctuidae). Environmental Entomology 29, 489–494.CrossRefGoogle Scholar
Fantinou, A.A., Tsitsipis, J.A. & Karandinos, M.G. (1998) Diapause termination in Sesamia nonagrioides (Lepidoptera, Noctuidae) under laboratory and field conditions. Environmental Entomology 27, 53–58.CrossRefGoogle 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.CrossRefGoogle Scholar
Fitt, G.P. (1989) The ecology of heliothis in relation to agroecosystems. Annual Review of Entomology 34, 17–52.CrossRefGoogle Scholar
Ge, F., Chen, F., Paralulee, M.N. & Yardim, E.N. (2005) Quantification of diapausing fourth generation and suicidal fifth generation cotton bollworm, Helicoverpa armigera, in cotton and corn in northern China. Entomologia Experimentalis et Applicata 116, 1–7.CrossRefGoogle Scholar
Hackett, D. & Gatehouse, A.G. (1982) Diapause in Heliothis armigera (Hübner) and H. fletcheri (Hardwick) (Lepidoptera: Noctuidae) in the Sudan Gezira. Bulletin of Entomological Research 72, 409–422.CrossRefGoogle Scholar
Hardwick, D.F. (1965). The corn earworm complex. Memoirs of the American Entomological Society 40, 1–247.Google Scholar
Henneberry, T.J. Jr., Butler, G.D. & Coudriet, D.L. (1993) Tobacco budworm (Lepidoptera: Noctuidae): Effects of temperature and photoperiod on larval and pupal development, larval mortality and induction of pupal diapause. Southwestern Entomologist 18, 269–279.Google Scholar
Izumi, Y., Anniwaer, K., Yoshida, H., Sonoda, S., Fujisaki, K. & Tsumuki, H. (2005) Comparison of cold hardiness and sugar content between diapausing and nondiapausing pupae of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Physiological Entomology 30, 36–41.CrossRefGoogle 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.CrossRefGoogle Scholar
Kay, I.R. (1982) The incidence and duration of pupal diapause in Heliothis armigera (Hübner) (Lepidoptera: Noctuidae) in southeast Queensland. Journal of the Australian Entomological Society 21, 263–266.CrossRefGoogle Scholar
Koštál, V. (2006) Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113–127.CrossRefGoogle ScholarPubMed
Kurban, A., Yoshida, H., Izumi, Y., Sonoda, S. & Tsumuki, H. (2005) Pupal diapause of Helicoverpa armigera: sensitive stage for photoperiodic induction. Applied Entomology and Zoology 40, 457–460.CrossRefGoogle Scholar
Kurban, A., Yoshida, H., Izumi, Y., Sonoda, S. & Tsumuki, H. (2007) Pupal diapause of Helicoverpa armigera: sensitive stage for thermal induction. Bulletin of Entomological Research 97, 219–223.CrossRefGoogle ScholarPubMed
Kurban, A., Yoshida, H., Izumi, Y., Sonoda, S. & Tsumuki, H. (2008) Cold hardiness and sugar content in photo-insensitive individuals of the cotton bollworm Helicoverpa armigera. Physiological Entomology 33, 251–256.CrossRefGoogle 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.CrossRefGoogle Scholar
Leather, S.R., Walters, K.F.A. & Bale, J.S. (1993) The Ecology of Insect Overwintering. New York, USA, Cambridge University Press.CrossRefGoogle Scholar
Liu, Z., Gong, P., Heckel, G.D., Wei, W., Sun, J. & Li, D. (2009) Effects of larval host plants on overwintering physiological dynamics and survival of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Journal of Insect Physiology 55, 1–9.CrossRefGoogle ScholarPubMed
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. Journal of Insect Physiology 56, 1863–1870.CrossRefGoogle ScholarPubMed
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
Milonas, P.G. & Savopoulou-Soultani, M. (2000) Diapause in the parasitoid Colpoclypeus florus (Hymenoptera: Eulophidae): role of photoperiod and temperature. Annals of the Entomological Society of America 93, 512–518.CrossRefGoogle Scholar
Milonas, P.G. & Savopoulou-Soultani, M. (2004) Diapause termination in overwintering larvae of a Greek strain of Adoxophyes orana (Lepidoptera: Tortricidae). Environmental Entomology 33, 513–519.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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., 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.CrossRefGoogle ScholarPubMed
Musolin, D.L., Numata, H. & Saulich, A.H. (2001) Timing of diapause induction outside the natural distribution range of a species: an outdoor experiment with the bean bug Riptortus clavatus. Entomologia Experimentalis et Applicata 100, 211–219.CrossRefGoogle Scholar
Pearson, E.O. (1958) The Insect Pests of Cotton in Tropical Africa. London, UK, Commonwealth Institute of Entomology.Google Scholar
Pullen, S.R., Meola, R.W. & Lopez, J.D. (1992) Temperature as a sole factor for diapause induction after pupation in Helicoverpa zea (Lepidoptera: Noctuidae). Environmental Entomology 21, 1404–1409.CrossRefGoogle 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.) (Lepideptera: Noctuidae). Applied Entomology and Zoology 34, 327–331.CrossRefGoogle Scholar
Qureshi, M.H., Murai, T., Yoshida, H., Shiraga, T. & Tsumuki, H. (2000) Population variation in diapause induction and termination of Helicoverpa armigera (Lepideptera: Noctuidae). Applied Entomology and Zoology 35, 357–360.CrossRefGoogle Scholar
Reed, W. (1965) Heliothis armigera (Hb.) (Noctuidae) in Western Tanganyika. I-Biology, with special reference to the pupal stage. Bulletin of Entomological Research 56, 117–125.CrossRefGoogle Scholar
Roach, S.H. & Adkisson, P.L. (1970) Role of photoperiod and temperature in the induction of pupal diapause in the bollworm, Heliothis zea. Journal of Insect Physiology 16, 1591–1597.CrossRefGoogle ScholarPubMed
Rowe, L. & Ludwig, D. (1991) Size and timing of metamorphosis in complex life histories: time constraints and variation. Ecology 72, 413–427.CrossRefGoogle Scholar
Roome, R.E. (1979) Pupal diapause in Heliothis armigera (Hübner) (Lepidoptera: Noctuidae) in Botswana: its regulation by environmental factors. Bulletin of Entomological Research 69, 149–160.CrossRefGoogle Scholar
Saunders, D.S. (1982) Insect Clocks. 2nd edn. Oxford, UK, Pergamon Press.Google Scholar
Shimizu, K. & Fujisaki, K. (2002) Sexual differences in diapause induction of the cotton bollworm, Helicoverpa armigera (Hb.) (Lepidoptera: Noctuidae). Applied Entomology and Zoology 37, 527–533.CrossRefGoogle Scholar
Shimizu, K. & Fujisaki, K. (2006) Geographic variation in diapause induction under constant and changing conditions in Helicoverpa armigera. Entomologia Experimentalis et Applicata 121, 253–260.CrossRefGoogle Scholar
Shumakov, E.M. & Yakhimovich, L.A. (1955) Morphological and histological peculiarities of the metamorphosis of the cotton bollworm (Choridea obsoleta F.) in connection with the phenomenon of diapause. Doklady of Akademy of Sciences USSR 101, 779–782.Google Scholar
Shimizu, K., Shimizu, K. & Fujisaki, K. (2006) Timing of diapause induction and overwintering success in the cotton bollworm Helicoverpa armigera (Hb.) (Lepidoptera: Noctuidae) under outdoor condition in temperate Japan. Applied Entomology and Zoology 41, 151–159.CrossRefGoogle Scholar
Smith, N.C. (1966) Insect Colonization and Mass Production. New York, USA, Academic Press.Google Scholar
Sokal, R.R. & Rohlf, F.J. (1995) Biometry. 3rd ed.New York, USA, Freeman.Google Scholar
SPSS Inc. (2006) SPSS 14 for Windows, user's guide. Chicago, IL, USA, SPSS, Inc.Google Scholar
Tauber, M.J., Tauber, C.A. & Masaki, S. (1986) Seasonal Adaptations of Insects. New York, USA, Oxford University Press.Google Scholar
Vaz Nuñes, M. (1998) Thermoperiodic responses in insects and mites simulated with the double circadian oscillator clock. Journal of Biological Rhythms 13, 461–470.CrossRefGoogle ScholarPubMed
Volkovich, T.A. & Blumental, N.A. (1997) Photo-thermoperiodic responses in some species of lacewings (Neuroptera: Chrysopidae): their role in diapause induction. European Journal of Entomology 94, 435–444.Google Scholar
Wang, X.P., Xue, F.S., Ge, F., Zhou, C.A. & You, L.S. (2004) Effects of thermoperiods on the diapause induction in the cabbage beetle, Colaphellus bowringi Baly (Coleoptera: Chrysomelidae). Physiological Entomology 29, 419–425.CrossRefGoogle Scholar
Wang, X.P., Xue, F.S., Zhou, X.M. & Lei, C.L. (2007) Thermoperiodic response and effect of photoperiod on thermoperiodic induction of diapause in Colaphellus bowringi. Entomologia Experimentalis et Applicata 124, 299–304.CrossRefGoogle Scholar
Wellso, S.G. & Adkisson, P.L. (1966) A long-day short-day effect in the photoperiodic control of the pupal diapause of the bollworm, Heliothis zea (Boddie). Journal of Insect Physiology 12, 1455–1465.CrossRefGoogle Scholar
Wilson, A.G.L., Lewis, T. & Cunningham, R.B. (1979) Overwintering and spring emergence of Heliothis armigera (Hübner) (Lepidoptera: Noctuidae) the Namoi Valley, New South Wales. Bulletin of Entomological Research 69, 97–109.CrossRefGoogle Scholar
Zalucki, M.P., Daglish, G., Firempong, S. & Twine, P.H. (1986) The biology and ecology of Heliothis armigera (Hübner) and H. punctigera Wallengren (Lepidoptera: Noctuidae) in Australia: what do we know? Australian Journal of Zoology 34, 779–814.CrossRefGoogle 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.CrossRefGoogle Scholar
Zhou, X., Applebaum, S.W. & Coll, M. (2000) Overwintering and spring migration in the bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) in Israel. Environmental Entomology 29, 1289–1294.CrossRefGoogle Scholar