Skip to main content
Log in

Effects of photoperiod, temperature and aging on adult diapause termination and post-diapause development in female Asian comma butterflies, Polygonia c-aureum Linnaeus (Lepidoptera: Nymphalidae)

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Polygonia c-aureum females exhibit photoperiodically induced imaginal diapause, characterized by cessation of ovarian development. Females grown at a short daylength (SD) entered imaginal diapause, whereas those grown at a long daylength (LD) produced eggs rapidly after adult emergence at 21 °C. The termination of diapause was influenced by daylength: diapause ended faster at LD than SD. Complete termination of diapause took 30 days in unchilled females reared under LD at 21 °C. On the other hand, prompt, synchronized and strong diapause termination occurred at post-chilling periods. Photoperiods at post-chilling periods affected ovarian development, when the length of pre-chilling periods or the length of chilling periods was shorter, suggesting that these treatments were not enough to complete diapause development. Ovarian development proceeded earlier in chilled and subsequent warmed females than unchilled females. Wing damage was remarkable at post-chilling periods when females were reared under an adequate length of pre-chilling and chilling periods, especially comparing with females under pre-overwintering conditions without chilling, indicating that post-diapause reproductive development was weak in unchilled females. Thus, exposure to low temperatures is necessary for a strong diapause termination in this butterfly.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Broufas GD, Pappas ML, Koveos DS (2006) Effect of cold exposure and photoperiod on diapause termination of the predatory mite Euseius finlandicus (Acari: Phytoseiidae). Environ Entomol 35:1216–1221

    Article  Google Scholar 

  • de Kort CAD (1990) Thirty-five years of diapause research with the Colorado potato beetle. Entomol Exp Appl 56:1–13

    Article  Google Scholar 

  • Endo K (1970a) Relation between accumulation of secretory fluid in the accessory gland of the female genital organ activity of the corpus allatum in Polygonia c-aureum L. Zool Mag 82:53–58 (in Japanese with English summary)

    Google Scholar 

  • Endo K (1970b) Relation between ovarian maturation and activity of the corpora allata in seasonal forms of the butterfly, Polygonia c-aureum L. Dev Growth Differ 11:297–304

    Article  CAS  Google Scholar 

  • Endo K (1973) Hormonal regulation of mating in the butterfly, Polygonia c-aureum L. Dev Growth Differ 15:1–10

    Article  Google Scholar 

  • Fantinou AA, Tsitsipisk JA, Karandinos MG (1998) Diapause termination in Sesamia nonagrioides (Lepidoptera: Noctuidae) under laboratory and field conditions. Environ Entomol 27:53–58

    Article  Google Scholar 

  • Fujita KM. Inoue M, Watanabe A, Islam TMF, Shahjahan RM, Endo K, Yamanaka A (2009) Photoperiodic regulation of reproductive activity in summer- and autumn-morph butterflies of Polygonia c-aureum L. Zool Stud 48:291–297

    Google Scholar 

  • Fukuda S, Endo K (1966) Hormonal control for the development of seasonal forms in the butterfly, Polygonia c-aureum L. Proc Jpn Acad 42:1082–1087

    Article  Google Scholar 

  • Han E-N, Bauce E (1996) Diapause development of spruce budworm larvae, Choristoneura fumiferana (Clem) (Lepidoptera: Tortricidae), at temperatures favoring post-diapause development. Can Entomol 128:167–169

    Article  Google Scholar 

  • Hidaka T, Aida S (1963) Day length as the main factor of seasonal form determination in Polygonia c-aureum (Lepidoptera, Nymphalidae). Zool Mag 72:77–83

    Google Scholar 

  • Hidaka T, Takahashi H (1967) Temperature conditions and maternal effect as modifying factors in photoperiodic control of the seasonal form in Polygonia c-aureum (Lepidoptera: Nymphalidae). Annot Zool Japon 40:200–204

    Google Scholar 

  • Hiroyoshi S (1992) Effects of photoperiod and temperature on several pupal characters associated with imaginal polyphenism in Polygonia c-aureum (Lepidoptera, Nymphalidae). Appl Entomol Zool 27:155–159

    Article  Google Scholar 

  • Hiroyoshi S, Reddy GVP, Mitsuhashi J (2017) Effects of juvenile hormone analogue (methoprene) and 20-hydroxyecdysone on reproduction in Polygonia c-aureum (Lepidoptera: Nymphalidae) in relation to adult diapause. J Comp Physiol A 203:635–647

    Article  CAS  Google Scholar 

  • Hodek I (1970) Termination of diapause in two Coccinellids (Coleoptera). Acta Entomol Bohemoslov 67:218–222

    Google Scholar 

  • Hodek I (1974) Reactivation of diapausing Aelia acuminate adults before hibernation (Heteroptera). Acta Entomol Bohemoslov 71:65–71

    Google Scholar 

  • Hodek I (1979) Intermittent character of adult diapause in Aelia acuninata (Heteroptera). J Insect Physiol 25:867–871

    Article  Google Scholar 

  • Hodek I (1999) Environmental regulation and some neglected aspects of insect diapause. Entomol Sci 2:533–537

    Google Scholar 

  • Hodek I (2002) Controversial aspects of diapause development. Eur J Entomol 99:163–173

    Article  Google Scholar 

  • Hodek I, Hodkova M (1988) Multiple role of temperature during insect diapause: a review. Entomol Exp Appl 49:153–165

    Article  Google Scholar 

  • Hodek I, Ruzicka Z (1977) Insensitivity to photoperiod after diapause in Semiadalia undecimnotata (Col.: Coceinellidae). Entomophaga 22:169–174

    Article  Google Scholar 

  • Hodek I, Hodkova M, Semyanov VP (1989) Physiological state of Coccinella septempunctata adults from northern Greece sampled in mid-hibernation. Acta Entomol Bohemoslov 86:241–251

    Google Scholar 

  • Hodkova M, Hodek I, Sommer L (1989) Cold in not prerequisite for the completion of photoperiodically induced diapause in Dolycoris baccarum from Norway. Entomol Exp Appl 52:185–188

    Article  Google Scholar 

  • Honěk A, Hodek I (1973) Diapause of Chrysopa carnea (Chrysopidae: Neuroptera) females in the field. Vestnik Ceskosl Spol Zool 37:95–100

    Google Scholar 

  • Jiang XF, Huang SH, Luo LZ, Zhang L (2010) Diapause termination, post-diapause development and reproduction in the beet webworm, Loxostege sticticalis (Lepidoptera: Pyralidae). J Insect Physiol 56:1325–1331

    Article  CAS  Google Scholar 

  • Koštάl V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113–127

    Article  Google Scholar 

  • Koštάl V, Tollarova M, Doležel D (2008) Dynamism in physiology and gene transcription during reproductive diapause in a heteropteran bug, Pyrrhocoris apterus. J Insect Physiol 54:77–88

    Article  Google Scholar 

  • Leather SR, Walters KFA, Bale JS (1993) The ecology of insect overwintering. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Leong KLH, Frey D, Hamaoka D, Honma K (1993) Wing damage in overwintering populations of monarch butterfly at two California sites. Ann Entomol Soc Am 86:728–733

    Article  Google Scholar 

  • Milonas PG, Savopoulou-Soultani M (2004) Diapause termination in overwintering larvae of a Greek strain of Adoxophyes orana (Lepidoptera: Tortricidae). Environ Entomol 33:513–519

    Article  Google Scholar 

  • Musolin DL, Fujisaki K, Numata H (2007) Photoperiodic control of diapause termination, colour change and postdiapause reproduction in the southern green stink bug, Nezara viridula. Physiol Entomol 32:64–72

    Article  Google Scholar 

  • Numata H, Hidaka T (1982) Photoperiodic control of adult diapause in the bean bug, Riptortus clavatus Thunberg (Heteroptera: Coreidae). I. Reversible induction and termination of diapause. Appl Entomol Zool 17:530–538

    Article  Google Scholar 

  • Propp GD, Tauber MJ, Tauber CA (1969) Diapause in the neuropteran Chrysopa oculata. J Insect Physiol 15:1749–1757

    Article  Google Scholar 

  • Raabe M (1986) Insect reproduction of successive steps. Advan Insect Physiol 19:29–154

    Article  CAS  Google Scholar 

  • Tauber MJ, Tauber CA (1973) Nutritional and photoperiodic control of the seasonal reproductive cycle in Chrysopa Mohave (Neuroptera). J Insect Physiol 19:729–736

    Article  CAS  Google Scholar 

  • Tauber MJ, Tauber CA (1974) Thermal accumulations, diapause and oviposition in a conifer-inhabiting predator, Chrysopa harrisii (Neuroptera). Can Entomol 106:969–978

    Article  Google Scholar 

  • Tauber MJ, Tauber CA (1976) Insect seasonality. Diapause maintenance, termination and post-diapause development. Ann Rev Entomol 21:81–107

    Article  Google Scholar 

  • Tauber MJ,. Tauber CA, Masaki S (1986) Seasonal adaptation of insects. Oxford University Press, New York

    Google Scholar 

  • Wada T, Kobayashi M (1985) Seasonal changes of wing wear of Cnaphalocrocis medinalis Guenee in paddy fields. Jpn J Appl Entomol Zool 29:41–44 (In Japanese.with English summary)

    Article  Google Scholar 

  • Watanabe M, Ando S (1993) Influence of mating frequency on lifetime fecundity I in wild females the small white Pieris rapae (Lepidoptera: Pieridae). Jpn J Entomol 61:691–696 (In Japanese with English summary)

    Google Scholar 

  • Watanabe M, Nakanishi Y (1996) Population structure and dispersals of the sulfur butterfly Colias erate (Lepidoptera: Pieridae) in an isolated plain located in a cool temperate zone of Japan. Jpn J Entomol 64:17–29 (In Japanese with English summary)

    Google Scholar 

  • Watt WB, Chew FS, Snyder LRG, Watt AG, Rothshild DE (1977) Population structure of pierid butterflies. I. Numbers and movements of some montane Colias species. Oecologia 27:1–22

    Article  Google Scholar 

  • Xiao H-J, Mou F-C, Zhu X-F, Xue F-S (2010) Diapause induction, maintenance and termination in the rice stem borer Chilo suppressalis (Walker). J Insect Physiol 56:1558–1564

    Article  CAS  Google Scholar 

  • Yang H-Z, Tu X-Y, Xia Q-W, He H-M, Chen C, Xue F-S (2014) Photoperiodism of diapause induction and diapause termination in Ostrinia furnacalis. Entomol Exp Appl 153:34–46

    Article  Google Scholar 

Download references

Acknowledgements

We thank for Dr. S. Tanaka of the National Institute of Agrobiological Sciences (NIAS) for critical reading of the manuscript. Thanks are also due to Dr. S. Moriya, Dr. K. Tateishi and Mr. K. Takashino for their help.

Author information

Authors and Affiliations

Authors

Ethics declarations

Human and animal rights

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animal were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hiroyoshi, S., Reddy, G.V.P. & Mitsuhashi, J. Effects of photoperiod, temperature and aging on adult diapause termination and post-diapause development in female Asian comma butterflies, Polygonia c-aureum Linnaeus (Lepidoptera: Nymphalidae). J Comp Physiol A 204, 849–858 (2018). https://doi.org/10.1007/s00359-018-1284-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-018-1284-y

Keywords

Navigation