Eur. J. Entomol. 119: 69-76, 2022 | DOI: 10.14411/eje.2022.007

Time measurement in insect photoperiodism: The role of photophase duration and light intensityIvo Hodek special issueReview

David SAUNDERS
21 Leadervale Road, Edinburgh EH16 6PB, Scotland, United Kingdom; e-mail: david59.saunders@mypostoffice.co.uk

The initial stages of diapause induction - as summer gives way to autumn - involve a process of time measurement in which the duration of daylength (or nightlength) is determined by a photoperiodic 'clock' based upon the circadian system. In many insects so far examined, a photophase of sufficient duration and illuminance resets a photoperiodic oscillator to a constant phase equivalent to the beginning of the 'subjective night' (Circadian time, CT 12 h) whereupon it proceeds to measure nightlength in a clock of the external coincidence type. A possible exception may be found in the linden bug, Pyrrhocoris apterus, which - in laboratory studies using relatively low light intensity - suggests that daylength is measured rather than the night. Earlier studies of photoperiodic responses (pupal diapause induction) in the flesh fly Sarcophaga argyrostoma, however, showed that 'weak' or short light pulses giving rise to Type 1 phase response curves could be converted by increasing light intensity to Type 0 responses that phase set the oscillation to the beginning of the subjective night (CT 12 h) whereupon it could begin to measure the night. Based upon these data it is therefore suggested that the photoperiodic clock in P. apterus might also measure nightlength if the bugs were exposed to photophases of higher irradiance simulating daytime exposure to the light intensity experienced by these diurnally active insects in their natural environment.

Keywords: Diapause, Pyrrhocoris apterus, day- or nightlength measurement

Received: December 5, 2021; Revised: January 13, 2022; Accepted: January 13, 2022; Published online: January 19, 2022  Show citation

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SAUNDERS, D. (2022). Time measurement in insect photoperiodism: The role of photophase duration and light intensity. EJE119, Article 69-76. https://doi.org/10.14411/eje.2022.007


This paper was contributed to a virtual special issue in memory of Ivo Hodek, a long-time editor of the European Journal of Entomo­logy, who died on June 11, 2021, shortly after his ninetieth birthday.


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References

  1. Andrewartha H.G. 1952: Diapause in relation to the ecology of insects. - Biol. Rev. 27: 50-107. Go to original source...
  2. Bünning E. 1935: Zur kenntnis der endogenen Tagesperiodizitat bei Insekten und Pflanzen. - Ber. Dt. Bot. Ges. 53: 594-623. Go to original source...
  3. Bünning E. 1936: Die endogene Tagesrhythmik als Grundlage der photoperiodischen Reaktion. - Ber. Dt. Bot. Ges. 54: 590-607. Go to original source...
  4. Bünning E. 1960: Circadian rhythms and time measurement in photoperiodism. - Cold Spring Harb. Symp. Quant. Biol. 25: 249-256. Go to original source...
  5. Chandrashekaran M.K. & Engelmann W. 1973: Early and late subjective night phases of the Drosophila pseudoobscura circadian rhythm require different energies of blue light for phase shifting. - Z. Naturforsch. 28C: 750-753. Go to original source...
  6. Chandrashekaran M.K. & Engelmann W. 1976: Amplitude attenuation of the circadian rhythm in Drosophila pseudoobscura with light pulses of varying irradiance and duration. - Int. J. Chronobiol. 4: 231-240.
  7. Chandrashekeran M.K. & Loher W. 1969: The relationship between the intensity of the light pulses and the extent of phase shifts of the circadian rhythm in the eclosion rate of Drosophila pseudoobscura. - J. Exp. Zool. 172: 147-152. Go to original source...
  8. Chovnick A. (ed.) 1960: Biological Clocks. Cold Spring Harbor Symp. Quant. Biol. Vol. 25. New York, 514 pp. Go to original source...
  9. Dickson R.C. 1949: Factors governing the induction of diapause in the oriental fruit moth. - Ann. Entomol. Soc. Am. 41: 511-537. Go to original source...
  10. Engelmann W. 1969: Phase shifting of eclosion in Drosophila pseudoobscura as a function of the energy of the light pulse. - Z. Vergl. Physiol. 64: 111-117. Go to original source...
  11. Garner W.W. & Allard H.A. 1920: Effects of the relative length of the day and night and other factors of the environment on growth and reproduction in plants. - J. Agric. Res. 18: 553-606. Go to original source...
  12. Goto S.G. & Numata H. 2009: Possible involvement of distinct photoreceptors in the photoperiodic induction of diapause in the flesh fly Sarcophaga similis. - J. Insect Physiol. 55: 401-407. Go to original source...
  13. Hodek I. 1971: Termination of adult diapause in Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae) in the field. - Entomol. Exp. Appl. 14: 212-222. Go to original source...
  14. Hodek I. 1999: Environmental regulation and some neglected aspects of insect diapause. - Entomol. Sci. 2: 533-537.
  15. Hodek I. 2002: Controversial aspects of diapause development. - Eur. J. Entomol. 99: 163-173. Go to original source...
  16. Kalmus H. 1935: Periodizität und Autochronie (Idiochronie) als Zeitregelnde Eigenschaffen der Organismen. - Biol. Gener. 11: 93-114.
  17. Kenny N.A.P. & Saunders D.S. 1991: Adult locomotor rhythmicity as "hands" of the maternal photoperiodic clock regulating larval diapause in the blowfly, Calliphora vicina. - J. Biol. Rhythms 6: 217-233. Go to original source...
  18. Kogure M. 1933: The influence of light and temperature on certain characters of the silkworm, Bombyx mori. - J. Dept. Agr. Kyushu Univ. 4: 1-93. Go to original source...
  19. Kotwica-Rolinska J., Pivarciova L., Vaneckova H. & Dolezel D. 2017: The role of circadian clock genes in the photoperiodic timer of the linden bug Pyrrhocoris apterus during the nymphal stage. - Physiol. Entomol. 42: 266-273. Go to original source...
  20. Lankinen P., Kastally C. & Hoikkala A. 2021: Nanda-Hamner curves show huge latitudinal variation but no circadian components in Drosophila montana photoperiodism. - J. Biol. Rhythms 20: 1-13. Go to original source...
  21. Lees A.D. 1965: Is there a circadian component in the Megoura photoperiodic clock? In Aschoff J. (ed.): Circadian Clocks.North-Holland, Amsterdam, pp. 351-356.
  22. Lees A.D. 1973: Photoperiodic time measurement in the aphid Megoura viciae. - J. Insect Physiol. 19: 2279-2316. Go to original source...
  23. Marcovitch S. 1923: Plant lice and light exposure. - Science 58: 537-538. Go to original source...
  24. Marcovitch S. 1924: The migration of the Aphididae and the appearance of sexual forms as affected by the relative length of daily light exposure. - J. Agric. Res. 27: 513-522.
  25. Mukai A., Yamaguchi K. & Goto S.G. 2021: Urban warming and artificial light alter dormancy in the flesh fly. - R. Soc. Open Sci. 8: 210866, 10 pp. Go to original source...
  26. Nanda K.K. & Hamner K.C. 1958: Studies on the nature of the endogenous rhythm affecting photoperiodic response of Biloxi soy bean. - Bot. Gaz. 120: 14-25. Go to original source...
  27. Norris K.H., Howell F., Hayes D.K., Adler V.E., Sullivan W.N. & Schechter M.S. 1969: The action spectrum for breaking diapause in the codling moth, Laspeyresia pomonella (L.), and the oak silkworm, Antheraea pernyi Guer. - Proc. Natl. Acad. Sci. USA 63: 1120-1127. Go to original source...
  28. Paris O.H. & Jenner C.E. 1959: Photoperiodic control of diapause in the pitcher-plant midge, Metriocnemus knabi. In Withrow R.B. (ed.): Photoperiodism and Related Phenomena in Plants and Animals. Am. Ass. Adv. Sci., Washington, pp. 601-624.
  29. Pittendrigh C.S. 1954: On temperature independence in the clock controlling emergence time in Drosophila. - Proc. Natn. Acad. Sci. USA 40: 1018-1029. Go to original source...
  30. Pittendrigh C.S. 1960: Circadian rhythms and the circadian organization of living systems. - Cold Spring Harb. Symp. Quant. Biol. 25: 159-184. Go to original source...
  31. Pittendrigh C.S. 1966: The circadian oscillation in Drosophila pseudoobscura pupae: a model for the photoperiodic clock. - Z. Pflanzenphysiol. 54: 275-307.
  32. Pittendrigh C.S. 1972: Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. - Proc. Natn. Acad. Sci. USA 69: 2734-2717. Go to original source...
  33. Sabrosky C.W., Larson I. & Nabours R.K. 1933: Experiments with light upon reproduction, growth and diapause in grouse locusts. - Trans. Kansas Acad. Sci. 36: 298-300. Go to original source...
  34. Saunders D.S. 1971: The temperature-compensated photoperiodic clock 'programming' development and pupal diapause in the flesh-fly, Sarcophaga argyrostoma. - J. Insect Physiol. 17: 801-812. Go to original source...
  35. Saunders D.S. 1973: The photoperiodic clock in the flesh-fly, Sarcophaga argyrostoma. - J. Insect Physiol. 19: 1941-1954. Go to original source...
  36. Saunders D.S. 1978: An experimental and theoretical analysis of photoperiodic induction in the flesh-fly Sarcophaga argyrostoma. - J. Comp. Physiol. (A) 124: 75-95. Go to original source...
  37. Saunders D.S. 1979: External coincidence and the photoinducible phase in the Sarcophaga photoperiodic clock. - J. Comp. Physiol. (A) 132: 179-189. Go to original source...
  38. Saunders D.S. 1982: The effect of ultra-short photoperiods on the seasonal clock in Sarcophaga argyrostoma. - J. Comp. Physiol. (A) 145: 421-429. Go to original source...
  39. Saunders D.S. 1983: A diapause induction-termination asymmetry in the photoperiodic responses of the linden bug, Pyrrhocoris apterus, and an effect of near-critical photoperiods on development. - J. Insect Physiol. 29: 399-405. Go to original source...
  40. Saunders D.S. 1987: Insect photoperiodism: the linden bug, Pyrrhocoris apterus, a species that measures daylength rather than nightlength. - Experientia 43: 935-937. Go to original source...
  41. Saunders D.S. 2013: Insect photoperiodism: measuring the night. - J. Insect Physiol. 59: 1-10. Go to original source...
  42. Saunders D.S. 2020: Dormancy, diapause, and the role of the circadian system in insect photoperiodism. - Annu. Rev. Entomol. 65: 19.1-19.17. Go to original source...
  43. Saunders D.S. 2021a: Insect photoperiodism: Bünning's hypothesis, the history and development of an idea. - Eur. J. Entomol. 118: 1-13. Go to original source...
  44. Saunders D.S. 2021b: A comparative study of circadian rhythmicity and photoperiodism in closely related species of blow flies: external coincidence, maternal induction and diapause at northern latitudes. - J. Biol. Rhythms 36: 532-547. Go to original source...
  45. Teets N.M. & Meuti M.E. 2021: Hello darkness, my old friend: a tutorial of Nanda-Hamner protocols. - J. Biol. Rhythms 36: 221-225. Go to original source...
  46. Vaz Nunes M. & Saunders D.S. 1999: Photoperiodic time measurement in insects: a review of clock models. - J. Biol. Rhythms 14: 84-104. Go to original source...
  47. Vaze K.M. & Helfrich-Forster C. 2016: Drosophila ezoana uses an hour-glass or highly damped circadian clock for measuring night length and inducing diapause. - Physiol. Entomol. 41: 378-389. Go to original source...
  48. Way M.J. & Hopkins B.A. 1950: The influence of photoperiod and temperature on the induction of diapause in Diataraxia ole­racea L. - J. Exp. Biol. 27: 365-376. Go to original source...
  49. Winfree A.T. 1970: Integrated view of resetting a circadian clock. - J. Theor. Biol. 28: 327-374. Go to original source...
  50. Winfree A.T. 1974: Suppressing Drosophila's circadian rhythm with dim light. - Science 183: 970-972. Go to original source...
  51. Winfree A.T. 1980: The Geometry of Biological Time. Springer, New York, Heidelberg, Berlin, 530 pp. Go to original source...

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