Advertisement

Circadian and Seasonal Timing of Insect Olfactory Systems

  • Sakiko ShigaEmail author
Chapter

Abstract

Insects are exposed to cyclic environmental changes caused by regular geophysical events. To cope with physical and biological changes, insects set their activities at an appropriate time of the day and of the year, causing daily rhythm and seasonal rhythm. Using photoperiod and temperature insects adjust their development and reproduction to favorable seasons, and overcome unfavorable ones to enter diapause. During active seasons insect behavior or activity is timed in a fixed period of a day by the circadian clock. Both photoperiodism and daily rhythms employ circadian clock mechanisms. For efficient insect control, consideration of biological timing system is important to determine timing for application of controlling agents or appropriate treatments.

References

  1. Anton S, Dufour MC, Gadenne C (2007) Plasticity of olfactory-guided behaviour and its neurobiological basis: lessons from moths and locusts. Entomol Exp Appl 123:1–11Google Scholar
  2. Beck SD (1980) Insect photoperiodism, 2nd edn. Academic, New York, p 387Google Scholar
  3. Bell RA, Rasul CG, Joachim FG (1975) Photoperiodic induction of the pupal diapause in the tobacco hornworm, Manduca sexta. J Insect Physiol 21:1471–1480Google Scholar
  4. Brown MR, Sieglaff DH, Rees HH (2009) Gonadal ecdysteroidogenesis in Arthropoda: occurrence and regulation. Annu Rev Entomol 54:105–125Google Scholar
  5. Chapman JW, Lim KA, Reynolds DR (2013) The significance of midsummer movements of Autographa gamma: implications for a mechanistic understanding of orientation behavior in a migrant moth. Curr Zool 59:360–370Google Scholar
  6. Colvin J, Gatehouse G (1993) Migration and genetic regulation of the prereproductive period in the cotton-bollworm moth, Helicoverpa armigera. Heredity 70:407–412Google Scholar
  7. Cusson M, McNeil JN (1989) Involvement of juvenile hormone in the regulation of pheromone release activities in a moth. Science 243:210–212Google Scholar
  8. DeCoursey PJ, Krulas JR, Mele G, Holley DC (1997) Circadian performance of suprachiasmatic nuclei (SCN)-lesioned antelope ground squirrels in a desert enclosure. Physiol Behav 62:1099–1108Google Scholar
  9. DeCoursey PJ, Walker JK, Smith SA (2000) A circadian pacemaker in free-living chipmunks: essential for survival? J Comp Physiol A 186:169–180Google Scholar
  10. Delisle J, McNeil JN (1986) The effect of photoperiod on the calling behaviour of virgin females of the true armyworm, Pseudaletia unipuncta (haw.) (lepidoptera: noctuidae). J Insect Physiol 32:199–206Google Scholar
  11. Delisle J, McNeil JN (1987) The combined effect of photoperiod and temperature on the calling behaviour of the true armyworm, Pseudaletia unipunct. Physiol Entomol 12:157–164Google Scholar
  12. Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122Google Scholar
  13. Denlinger DL, Yocum GD, Rinehart JP (2012) Hormonal control of diapause. In: Gilbert LI (ed) Insect endocrinology. Elsevier BV Academic Press, Waltham, pp 430–463Google Scholar
  14. Dolezel D (2014) Photoperiodic time measurement in insects. Curr Opin Insect Sci 7:1–6Google Scholar
  15. Endo N, Wada T, Sasaki R (2011) Seasonal synchrony between pheromone trap catches of the bean bug, Riptortus pedestris (Heteroptera: Alydidae) and the timing of invasion of soybean fields. Appl Entomol Zool 46:477–482Google Scholar
  16. Fukuda S (1940) Determination of the voltinism in the silkworm with special reference to the pigment formation in the serosa of the egg. Zool Mag 52:415–429Google Scholar
  17. Gadenne C (1993) Effects of fenoxycarb, juvenile hormone mimetic, on female sexual behavior of the black cutworm, Agrotis ipsilon (Lepidoptera: Noctuidae). J Insect Physiol 39:721–724Google Scholar
  18. Gadenne C, Renou M, Sreng L (1993) Hormonal control of pheromone responsiveness in the male black cutworm Agrotis ipsilon. Experientia 49:721–724Google Scholar
  19. Gatehouse AG, Zhang XX (1995) Migratory potential of insects: variation in an uncertain environment. In: Drake VA, Gatehouse AG (eds) Insect migration: tracking resource in space and time. Cambridge University Press, Cambridge, pp 193–242Google Scholar
  20. Gemeno C, Haynes KF (2001) Impact of photoperiod on the sexual behavior of the black cutworm moth (Lepidoptera: Noctuidae). Environ Entomol 30:189–195Google Scholar
  21. Goehring L, Oberhauser L (2002) Effects of photoperiod, temperature, and host plant ager on induction of reproductive diapause and development time in Danaus plexippus. Ecol Entomol 27:674–685Google Scholar
  22. Goto SG (2013) Roles of circadian clock genes in insect photoperiodism. Entomol Sci 16:1–16Google Scholar
  23. Greiner B, Gadenne C, Anton S (2002) Central processing of plant volatiles in Agrotis ipsilon males is age independent in contrast to sex pheromone processing. Chem Senses 27:45–48Google Scholar
  24. Groot AT (2014) Circadian rhythms of sexual activities in moths: a review. Front Ecol Evol 2:43Google Scholar
  25. Gruwez G, Hoste C, Lints CV, Lints FA (1971) Oviposition rhythms in Drosophila melanogaster and its alteration by a change in the photoperiodicity. Experientia 27:1414–1416Google Scholar
  26. Han EN, Gatehouse G (1991) Effects of temperature and photoperiod on the calling behavior of a migratory insect, the oriental armyworm Mythimna separata. Physiol Entomol 16:419–427Google Scholar
  27. Hardeland R (1972) Species differences in the diurnal rhythmicity of courtship behavior within the melanogaster group of the genus Drosophila. Anim Behav 20:170–174Google Scholar
  28. Helfrich-Förster C (2003) The neuroarchitecture of the circadian clock in the brain of Drosophila melanogaster. Microsc Res Tech 62(2):94–102Google Scholar
  29. Ichinose T (1974) Pupal diapause in some Japanese papilionid butterflies, with special reference to the difference in photoperiodic response between the diapausing pupae of Papilio maakii tutanus Fenton and P. xuthus Linnaeus. Kontyu 42:439–450Google Scholar
  30. Ikeno T, Tanaka SI, Numata H, Goto SG (2010) Photoperiodic diapause under the control of circadian clock genes in an insect. BMC Biol 8:116Google Scholar
  31. Johnson CG (1963) Physiological factors in insect migration by flight. Nature 198:423–427Google Scholar
  32. Kawasaki Y, Nishimura H, Shiga S (2017) Plausible link between circa‘bi’dian activity rhythms and circadian clock systems in the large black chafer Holotrichia parallela. J Exp Biol 220:4024–4034Google Scholar
  33. Kennedy JS (1961) A turning point in the study of insect migration. Nature 189:785–791Google Scholar
  34. Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 68:2112–2116Google Scholar
  35. Krishnan B, Dryer SE, Hardin PE (1999) Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 400:375–378Google Scholar
  36. Leal WS, Sawada M, Matsuyama S, Kuwahara Y, Hasegawa M (1993) Unusual periodicity of sex pheromone production in the large black chafer Holotrichia parallela. J Chem Ecol 19:1381–1391Google Scholar
  37. Leal WS, Higuchi H, Mizutani N, Nakamori H, Kadosawa T, Ono M (1995) Multifunctional communication in Riptortus clavatus (Heteroptera: Alydidae): conspecific nymphs and egg parasitoid Ooencyrtus nezarae use the same adult attractant pheromone as chemical cue. J Chem Ecol 21:973–985Google Scholar
  38. Li GB, Wang HX, Hu WX (1964) Route of the seasonal migration of the oriental armyworm moth in the eastern part of China as indicated by a three-year result of releasing and recapturing of marked moths. Act Phytophyl Sin 3:101–110Google Scholar
  39. McNeil JN (1986) Calling behavior: can it be used to identify migratory species of moths? Fla Entomol 69:78–84Google Scholar
  40. McNeil JN, Delisle J, Cusson M (1997) Regulation of pheromone production in Lepidoptera: the need for an ecological perspective. In: Cardé RT, Minks AD (eds) Insect pheromone research. Springer, Boston, pp 31–41Google Scholar
  41. Menon A, Varma V, Sharma VK (2014) Rhythmic egg-laying behaviour in virgin females of fruit flies Drosophila melanogaster. Chronobiol Int 31:433–441Google Scholar
  42. Merlin C, Lucas P, Rochat D, François MC, Maïbèche-Coisne M, Jacquin-Joly E (2007) An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis. J Biol Rhythm 22:502–514Google Scholar
  43. Mizutani N, Yasuda T, Yamaguchi T, Moriya S (2008) Pheromone contents and physiological conditions of adult bean bugs, Riptortus pedestris (Heteroptera: Alydidae), attracted to conspecific males during nondiapause and diapause periods in fields. Appl Entomol Zool 43:331–339Google Scholar
  44. Nishiitsutsuji-Uwo J, Pittendrigh CS (1968) Central nervous system control of circadian rhythmicity in the cockroach. III. The optic lobes, locus of the driving oscillation? Zeitsch Verg Physiol 58:14–46Google Scholar
  45. Page TL (1982) Transplantation of the cockroach circadian pacemaker. Science 216:73–75Google Scholar
  46. Page TL, Koelling E (2003) Circadian rhythm in olfactory response in the antennae controlled by the optic lobe in the cockroach. J Insect Physiol 49:697–707Google Scholar
  47. Pavelka J, Shimada K, Kostal V (2003) Timeless: a link between fly’s circadian and photoperiodic clocks? Eur J Entomol 100:255–265Google Scholar
  48. Perez SM, Taylor OR (2004) Monarch butterflies’ (Danaus plexippus) migratory behavior persists despite changes in environmental conditions. In: Oberhauser KS, Solensky M (eds) Monarch butterflies: ecology and population biology. Cornell University Press, Ithaca, pp 85–88Google Scholar
  49. Picimbon JF, Bécard JM, Sreng L, Clément JL, Gadenne C (1995) Juvenile hormone stimulates pheromonotropic brain factor release in the female black cutworm, Agrotis ipsilon. J Insect Physiol 41:377–382Google Scholar
  50. Plautz JD, Kaneko M, Hall JC, Kay SA (1997) Independent photoreceptive circadian clocks throughout Drosophila. Science 278:1632–1635Google Scholar
  51. Rabb RL (1966) Diapause in Protoparce sexta (Lepidoptera: Sphingidae). Ann Entomol Soc Am 59:160–165Google Scholar
  52. Rahman MM, Lim UT (2016) Females of Riptortus pedestris (Hemiptera: Alydidae) in reproductive diapause are more responsive to synthetic aggregation pheromone. J Econ Entomol 109:2082–2089Google Scholar
  53. Rosén WQ, Han GB, Löfstedt C (2003) The circadian rhythm of the sex-pheromone-mediated behavioral response in the turnip moth, Agrotis segetum, is not controlled at the peripheral level. J Biol Rhythm 18:402–408Google Scholar
  54. Roth LM, Barth RH (1967) The sense organs employed by cockroaches in mating behavior. Behaviour 28:58–93Google Scholar
  55. Rymer J, Bauernfeind AL, Brown S, Page TL (2007) Circadian rhythms in the mating behavior of the cockroach, Leucophaea maderae. J Biol Rhythm 22:43–57Google Scholar
  56. Saifullah ASM, Page TL (2009) Circadian regulation of olfactory receptor neurons in the cockroach antenna. J Biol Rhythm 24:144–152Google Scholar
  57. Sakai T, Ishida N (2001) Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc Natl Acad Sci U S A 98:9221–9225Google Scholar
  58. Sakamoto T, Uryu O, Tomioka K (2009) The clock gene period plays an essential role in photoperiodic control of nymphal development in the cricket Modicogryllus siamensis. J Biol Rhythm 24:379–390Google Scholar
  59. Sandrelli F, Costa R, Kyriacou CP, Rosato E (2008) Comparative analysis of circadian clock genes in insects. Insect Mol Biol 17:447–463Google Scholar
  60. Saunders DS (2002) Insect clocks, 3rd edn. Elsevier Science, Amsterdam, p 576Google Scholar
  61. Saunders DS (2009) Photoperiodism in insects: migration and diapause responses. In: Nelson RJ, Denlinger DL, Somers DE (eds) Photoperiodism: the biological calendar. Oxford University Press, Oxford, pp 218–257Google Scholar
  62. Schöfl G, Dill A, Heckel DG, Groot AT (2011) Allochronic separation versus mate choice: nonrandom patterns of mating between fall armyworm host strains. Am Nat 177:470–485Google Scholar
  63. Shiga S, Numata H (2009) Roles of PERIOD immunoreactive neurons in circadian rhythms and photoperiodism in the blow fly, Protophormia terraenovae. J Exp Biol 212:867–877Google Scholar
  64. Showers WB (1997) Migratory ecology of the black cutworm. Annu Rev Entomol 42:393–425Google Scholar
  65. Silvegren G, Löfstedt C, Rosén WQ (2005) Circadian mating activity and effect of pheromone pre-exposure on pheromone response rhythms in the moth Spodoptera littoralis. J Insect Physiol 51:277–286Google Scholar
  66. Somers J, Harper REF, Albert JT (2018) How many clocks, how many times? On the sensory basis and computational challenges of circadian systems. Front Behav Neurosci 12:211Google Scholar
  67. Sreng L (1993) Cockroach mating behaviors, sex pheromones, and abdominal glands (Dictyoptera: Blaberidae). J Insect Behav 6:715–735Google Scholar
  68. Tanoue S, Krishnan P, Krishnan B, Dryer SE, Hardin PE (2004) Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr Biol 14:638–649Google Scholar
  69. Tanoue S, Krishnan P, Chatterjee A, Hardin PE (2008) G protein-coupled receptor kinase 2 is required for rhythmic olfactory responses in Drosophila. Curr Biol 18:787–794Google Scholar
  70. Tomioka K, Chiba Y (1982) Persistence of circadian ERG rhythm in the cricket with optic tract severed. Naturwissenschaften 69:395–396Google Scholar
  71. Tomioka K, Chiba Y (1984) Effects of nymphal stage optic nerve severance or optic lobe removal on the circadian locomotor rhythm of the cricket, Gryllus bimaculatus. Zool Sci 1:375–382Google Scholar
  72. Tomioka K, Matsumoto A (2015) Circadian molecular clockworks in non-model insects. Curr Opin Insect Sci 7:58–64Google Scholar
  73. Turgeon J, McNeil JN (1982) Calling behavior of the armyworm, Pseudaletia unipuncta. Entomol Exp Appl 31:402–408Google Scholar
  74. Urquhart FA, Urquhart NR (1978) Autumnal migration routes of eastern population of monarch butterfly (Danaus p plexippus L., Danaidae; Lepidoptera) in North America to overwintering site in Neovolcanic Plateau of Mexico. Can J Zool 56:1759–1764Google Scholar
  75. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York, p 794Google Scholar
  76. Williams CB, Cockbill GF, Gibbs MA, Downes JA (1942) Studies in the migration of Lepidoptera. Trans R Ent Soc Lond 92:101–174Google Scholar
  77. Xia QW, Chen C, Tu XY, Yang HZ, Xue FS (2012) Inheritance of photoperiodic induction of larval diapause in the Asian corn borer Ostrinia furnacalis. Physiol Entomol 37:185–191Google Scholar
  78. Yasuda T, Mizutani N, Endo N, Fukuda T, Matsuyama R, Ito K, Moriya S, Sasaki R (2007a) A new component of attractive aggregation pheromone in the bean bug, Riptortus clavatus (Thunberg) (Heteroptera: Alydidae). Appl Entomol Zool 42:1–7Google Scholar
  79. Yasuda T, Mizutani N, Honda Y, Endo N, Yamaguchi T, Moriya S, Fukuda T, Sasaki R (2007b) A supplemental component of aggregation attractant pheromone in the bean bug Riptortus clavatus (Thunberg), related to food exploitation. Appl Entomol Zool 42:161–166Google Scholar
  80. Yoshioka K, Yamasaki Y (1984) Biology of Lachnosterna morosa Waterhouse and damages on taro. Jap J Appl Entomol Zool 38:5–8Google Scholar
  81. Zhao XC, Feng HQ, Wu B, Wu XF, Liu ZF, Wu KM, McNeil JN (2009) Does the onset of sexual maturation terminate the expression of migratory behavior in moths? A study of the oriental armyworm, Mythimna separata. J Insect Physiol 55:1039–1043Google Scholar
  82. Zhu H, Gegear RJ, Casselman A, Kanginakudru S, Reppert SM (2009) Defining behavioral and molecular differences between summer and migratory monarch butterflies. BMC Biol 7:14Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Biological ScienceOsaka UniverisityToyonakaJapan

Personalised recommendations