Journal of Comparative Physiology A

, Volume 204, Issue 9–10, pp 849–858 | Cite as

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)

  • Satoshi Hiroyoshi
  • Gadi V. P. Reddy
  • Jun Mitsuhashi
Original Paper


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.


Chilling Lepidoptera Ovary Reproduction Wing damage 



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.

Compliance with ethical standards

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.


  1. 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 35:1216–1221CrossRefGoogle Scholar
  2. de Kort CAD (1990) Thirty-five years of diapause research with the Colorado potato beetle. Entomol Exp Appl 56:1–13CrossRefGoogle Scholar
  3. 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
  4. 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 11:297–304CrossRefGoogle Scholar
  5. Endo K (1973) Hormonal regulation of mating in the butterfly, Polygonia c-aureum L. Dev Growth Differ 15:1–10CrossRefGoogle Scholar
  6. Fantinou AA, Tsitsipisk JA, Karandinos MG (1998) Diapause termination in Sesamia nonagrioides (Lepidoptera: Noctuidae) under laboratory and field conditions. Environ Entomol 27:53–58CrossRefGoogle Scholar
  7. 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 48:291–297Google Scholar
  8. Fukuda S, Endo K (1966) Hormonal control for the development of seasonal forms in the butterfly, Polygonia c-aureum L. Proc Jpn Acad 42:1082–1087CrossRefGoogle Scholar
  9. 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 128:167–169CrossRefGoogle Scholar
  10. Hidaka T, Aida S (1963) Day length as the main factor of seasonal form determination in Polygonia c-aureum (Lepidoptera, Nymphalidae). Zool Mag 72:77–83Google Scholar
  11. 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 40:200–204Google Scholar
  12. 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 27:155–159CrossRefGoogle Scholar
  13. 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 203:635–647CrossRefGoogle Scholar
  14. Hodek I (1970) Termination of diapause in two Coccinellids (Coleoptera). Acta Entomol Bohemoslov 67:218–222Google Scholar
  15. Hodek I (1974) Reactivation of diapausing Aelia acuminate adults before hibernation (Heteroptera). Acta Entomol Bohemoslov 71:65–71Google Scholar
  16. Hodek I (1979) Intermittent character of adult diapause in Aelia acuninata (Heteroptera). J Insect Physiol 25:867–871CrossRefGoogle Scholar
  17. Hodek I (1999) Environmental regulation and some neglected aspects of insect diapause. Entomol Sci 2:533–537Google Scholar
  18. Hodek I (2002) Controversial aspects of diapause development. Eur J Entomol 99:163–173CrossRefGoogle Scholar
  19. Hodek I, Hodkova M (1988) Multiple role of temperature during insect diapause: a review. Entomol Exp Appl 49:153–165CrossRefGoogle Scholar
  20. Hodek I, Ruzicka Z (1977) Insensitivity to photoperiod after diapause in Semiadalia undecimnotata (Col.: Coceinellidae). Entomophaga 22:169–174CrossRefGoogle Scholar
  21. Hodek I, Hodkova M, Semyanov VP (1989) Physiological state of Coccinella septempunctata adults from northern Greece sampled in mid-hibernation. Acta Entomol Bohemoslov 86:241–251Google Scholar
  22. 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 52:185–188CrossRefGoogle Scholar
  23. Honěk A, Hodek I (1973) Diapause of Chrysopa carnea (Chrysopidae: Neuroptera) females in the field. Vestnik Ceskosl Spol Zool 37:95–100Google Scholar
  24. 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 56:1325–1331CrossRefGoogle Scholar
  25. Koštάl V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113–127CrossRefGoogle Scholar
  26. 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 54:77–88CrossRefGoogle Scholar
  27. Leather SR, Walters KFA, Bale JS (1993) The ecology of insect overwintering. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  28. 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 86:728–733CrossRefGoogle Scholar
  29. Milonas PG, Savopoulou-Soultani M (2004) Diapause termination in overwintering larvae of a Greek strain of Adoxophyes orana (Lepidoptera: Tortricidae). Environ Entomol 33:513–519CrossRefGoogle Scholar
  30. 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 32:64–72CrossRefGoogle Scholar
  31. 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 17:530–538CrossRefGoogle Scholar
  32. Propp GD, Tauber MJ, Tauber CA (1969) Diapause in the neuropteran Chrysopa oculata. J Insect Physiol 15:1749–1757CrossRefGoogle Scholar
  33. Raabe M (1986) Insect reproduction of successive steps. Advan Insect Physiol 19:29–154CrossRefGoogle Scholar
  34. Tauber MJ, Tauber CA (1973) Nutritional and photoperiodic control of the seasonal reproductive cycle in Chrysopa Mohave (Neuroptera). J Insect Physiol 19:729–736CrossRefGoogle Scholar
  35. Tauber MJ, Tauber CA (1974) Thermal accumulations, diapause and oviposition in a conifer-inhabiting predator, Chrysopa harrisii (Neuroptera). Can Entomol 106:969–978CrossRefGoogle Scholar
  36. Tauber MJ, Tauber CA (1976) Insect seasonality. Diapause maintenance, termination and post-diapause development. Ann Rev Entomol 21:81–107CrossRefGoogle Scholar
  37. Tauber MJ,. Tauber CA, Masaki S (1986) Seasonal adaptation of insects. Oxford University Press, New YorkGoogle Scholar
  38. 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)CrossRefGoogle Scholar
  39. 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
  40. 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
  41. 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 27:1–22CrossRefGoogle Scholar
  42. 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 56:1558–1564CrossRefGoogle Scholar
  43. 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 153:34–46CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Applied Entomology, Faculty of AgricultureTokyo University of Agriculture and TechnologyFuchuJapan
  2. 2.KawagoeJapan
  3. 3.Department of Research Centers, Western Triangle Agricultural Research CenterMontana State UniversityConradUSA
  4. 4.BunkyoukuJapan

Personalised recommendations