Circadian rhythms of some behaviors of the cockroach Periplaneta americana L. (Blattodea, Blattidae) during ocelli shielding

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

In cockroaches the main role in the adjustment of circadian rhythms is attributed to the compound eyes; at the same time, morphological data indicate a possible role of ocelli in the modulation of the biological clock. Data obtained in this study reveal the effect of shielding the ocelli with black dye on the speed of the rhythm shift and its amplitude. In addition, it is shown that sexual behavior, locomotor activity, shelter occupation, and sleep-like behavior expressed as freezings, have a pronounced rhythm with a single peak, and resting periods have two pronounced minima at the beginning and at the end of the dark phase. Light intensity during the day phase affects the amplitude of behavioral rhythms in a manner similar to ocelli shielding.

About the authors

E. S. Novikova

Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences

Email: os_sacrum@list.ru
44 Toretz Ave., St. Petersburg, 194223 Russia

A. A. Puyto

Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences

Email: puyto.a@mail.ru
44 Toretz Ave., St. Petersburg, 194223 Russia

M. I. Zhukovskaya

Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences

Email: mzhukovskaya@rambler.ru
44 Toretz Ave., St. Petersburg, 194223 Russia

References

  1. Новикова Е. С., Жуковская М. И. 2017. Реакция замирания под действием яркого света у американского таракана, Periplaneta americana. Сенсорные системы 31 (1): 44–50.
  2. Новикова Е. С., Скиба Б. О., Пуйто А. А., Астахова Л. А., Ротов А. Ю., Жуковская М. И. 2025. Изменения электроретинограммы сложных глаз таракана Рeriplaneta americana L. при экранировании оцеллей. Сенсорные системы 39 (2): 75–87. doi: 10.31857/S0235009225020032
  3. Arnold T., Korek S., Massah A., Eschstruth D., Stengl M. 2020. Candidates for photic entrainment pathways to the circadian clock via optic lobe neuropils in the Madeira cockroach. Journal of Comparative Neurology 528 (10): 1754–1774. https://doi.org/10.1002/cne.24844
  4. Aschoff J. 1979. Circadian rhythms: influences of internal and external factors on the period measured in constant conditions. Zeitschrift für Tierpsychologie 49 (3): 225–249. https://doi.org/10.1111/j.1439-0310.1979.tb00290.x
  5. Aschoff J. 1981. A survey on biological rhythms. In: J. Aschoff (ed.). Biological Rhythms. Boston MA: Springer, p. 3–10. https://doi.org/10.1007/978-1-4615-6552-9_1
  6. Astakhova L. A., Novoselov A. D., Ermolaeva M. E., Firsov M. L., Rotov A. Y. 2021. Phototransduction in anuran green rods: origins of extra-sensitivity. International Journal of Molecular Sciences 22 (24): 13400. https://doi.org/10.3390/ijms222413400
  7. Ball H. J. 1971. The receptor site for photic entrainment of circadian rhythms in the cockroach Periplaneta americana. Annals of the Entomological Society of America 64: 1010–1015. https://doi.org/10.1093/aesa/64.5.1010
  8. Brown L. A., Fisk A. S., Pothecary C. A., Peirson S. N. 2019. Telling the time with a broken clock: quantifying circadian disruption in animal models. Biology 8 (1): 18. https://doi.org/10.3390/biology8010018
  9. Dolezelova E., Dolezel D., Hall J. C. 2007. Rhythm defects caused by newly engineered null mutations in Drosophila’s cryptochrome gene. Genetics 177: 329–345. https://doi.org/10.1534/genetics.107.076513
  10. Dreisig H. 1978. The circadian rhythm of bioluminescence in the glowworm, Lampyris noctiluca L. (Coleoptera, Lampyridae). Behavioral Ecology and Sociobiology 3: 1–18. https://doi.org/10.1007/BF00300044
  11. Enright J. T. 1965. The search for rhythmicity in biological time-series. Journal of Theoretical Biology 8 (3): 426–468. https://doi.org/10.1016/0022-5193(65)90021-4
  12. Goto S. G. 2022. Photoperiodic time measurement, photoreception, and circadian clocks in insect photoperiodism. Applied Entomology and Zoology 57 (3): 193–212. https://doi.org/10.1007/s13355-022-00785-7
  13. Hausl-Hofstätter U. 2008. Beobachtungen an nachtruhenden Hymenopteren in der Umgebung von Mali Lošinj, Kroatien (Anthophoridae, Andrenidae, Eumenidae, Scoliidae, Ichneumonidae). Joannea Zoologie 10: 101–21.
  14. Helfrich-Förster C. 2020. Light input pathways to the circadian clock of insects with an emphasis on the fruit fly Drosophila melanogaster. Journal of Comparative Physiology A 206 (2): 259–272. https://doi.org/10.1007/s00359-019-01379-5
  15. Hendricks J. C., Finn S. M., Panckeri K. A., Chavkin J., Williams J. A., Sehgal A., Pack A. I. 2000. Rest in Drosophila is a sleep-like state. Neuron 25 (1): 129–138. https://doi.org/10.1016/S0896-6273(00)80877-6
  16. Herrero M. J., Madrid J. A., Sánchez-Vázquez F. J. 2003. Entrainment to light of circadian activity rhythms in tench (Tinca tinca). Chronobiology International 20 (6): 1001–1017. 10.1081/cbi-120025246' target='_blank'>https://doi: 10.1081/cbi-120025246
  17. Honkanen A., Saari P., Takalo J., Heimonen K., Weckström M. 2018. The role of ocelli in cockroach optomotor performance. Journal of Comparative Physiology A 204 (2): 231–243. https://doi.org/10.1007/s00359-017-1235-z
  18. Kaiser W. 1988. Busy bees need rest, too. Journal of Comparative Physiology A 163 (5): 565–584. https://doi.org/10.1007/BF00603841
  19. Klein B. A. et al. 2008. Caste-dependent sleep of worker honey bees. Journal of Experimental Biology 211 (18): 3028–3040. https://doi.org/10.1242/jeb.017426
  20. Kutaragi Y., Tokuoka A., Tomiyama Y. et al. 2018. A novel photic entrainment mechanism for the circadian clock in an insect: involvement of c-fos and cryptochromes. Zoological Letters 4: 26. https://doi.org/10.1186/s40851-018-0109-8
  21. Levy K. et al. 2024. Crickets in the spotlight: exploring the impact of light on circadian behavior. Journal of Comparative Physiology A 210 (2): 267–279. https://doi.org/10.1007/s00359-023-01686-y
  22. Lin T. M., Lee H. J. 1996. The expression of locomotor orcadian rhythm in female German cockroach, Blattella germanica (L.). Chronobiology International 13 (2): 81–91. https://doi.org/10.3109/07420529609037072
  23. Lipton G. R., Sutherland D. J. 1970. Activity rhythms in the American cockroach, Periplaneta americana. Journal of Insect Physiology 16 (8): 1555–1566. https://doi.org/10.1016/0022-1910(70)90254-4
  24. Mizunami M. 1995. Functional diversity of neural organization in insect ocellar systems. Vision Research 35: 443–452. https://doi.org/10.1016/0042-6989(94)00192-O
  25. Mizunami M., Tateda H. 1986. Classification of ocellar interneurones in the cockroach brain. Journal of Experimental Biology 125 (1): 57–70. https://doi.org/10.1242/jeb.125.1.57
  26. Mote M. I., Black K. R. Action spectrum and threshold sensitivity of entrainment of circadian running activity in the cockroach Periplaneta americana. Photochemistry and Photobiology 34 (2): 257–265. https://doi.org/10.1111/j.1751-1097.1981.tb08995.x
  27. Mrosovsky N. 1999. Masking: history, definitions, and measurement. Chronobiology International 16 (4): 415–429. https://doi.org/10.3109/07420529908998717
  28. Nishiitsutsuji-Uwo J., Pittendrigh C. S. 1968. Central nervous system control of circadian rhythmicity in the cockroach: III. The optic lobes, locus of the driving oscillation? Zeitschrift für Vergleichende Physiologie 58: 14–46. https://doi.org/10.1007/BF00302434
  29. Okada Y., Tomioka K., Chiba Y. 1991. Circadian phase-response curves for light in nymphal and adult crickets, Gryllus bimaculatus. Journal of Insect Physiology 37 (8): 583–590. https://doi.org/10.1016/0022-1910(91)90035-X
  30. Page T. L. 1982. Transplantation of the cockroach circadian pacemaker. Science 216: 73–75. https://doi.org/10.1126/science.216.4541.73
  31. Page T. L., Barrett R. K. 1989. Effects of light on circadian pacemaker development: II. Responses to light. Journal of Comparative Physiology A 165: 51–59. https://doi.org/10.1007/BF00613799
  32. Page T. L., Caldarola P. C., Pittendrigh C. S. 1977. Mutual entrainment of bilaterally distributed circadian pacemaker. Proceedings of the National Academy of Sciences 74 (3): 1277–1281. https://doi.org/10.1073/pnas.74.3.1277
  33. Reischig T., Stengl M. 2003. Ectopic transplantation of the accessory medulla restores circadian locomotor rhythms in arrhythmic cockroaches (Leucophaea maderae). Journal of Experimental Biology 206 (11): 1877–1886. https://doi.org/10.1242/jeb.00373
  34. Rieger D., Stanewsky R., Helfrich-Förster C. 2003. Cryptochrome, compound eyes, Hofbauer–Buchner eyelets, and ocelli play different roles in the entrainment and masking pathway of the locomotor activity rhythm in the fruit fly Drosophila melanogaster. Journal of Biological Rhythms 18 (5): 377–391. https://doi.org/10.1177/0748730403256997
  35. Rivault C. 1976. The role of the eyes and ocelli in the initiation of circadian activity rhythms in cockroaches. Physiological Entomology 1 (4): 277–286. https://doi.org/10.1111/j.1365-3032.1976.tb00977.x
  36. Roberts S. K. 1974. Circadian rhythms in cockroaches: effects of optic lobe lesions. Journal of Comparative Physiology 88 (1): 21–30. https://doi.org/10.1007/BF00695920
  37. Ruf T. 1999. The Lomb–Scargle periodogram in biological rhythm research: Analysis of incomplete and unequally spaced time-series. Biological Rhythm Research 30 (2): 178–201. https://dx.doi.org/10.1076/brhm.30.2.178.1422
  38. Saunders D. S. 1997. Insect circadian rhythms and photoperiodism. Invertebrate Neuroscience 3: 155–164. https://doi.org/10.1007/BF02480370
  39. Saunders D. S. 2012. Insect photoperiodism: seeing the light. Physiological Entomology 37 (3): 207–218. https://doi.org/10.1111/j.1365-3032.2012.00837.x
  40. Schmid B., Helfrich-Förster C., Yoshii T. 2011. A new ImageJ plug-in “ActogramJ” for chronobiological analyses. Journal of Biological Rhythms 26 (5): 464–467. https://doi.org/10.1177/0748730411414264
  41. Sinam B., Sharma S., Thakurdas P. et al. 2012. Bright photophase accelerates re-entrainment after experimental jetlag in Drosophila. Naturwissenschaften 99: 575–578. https://doi.org/10.1007/s00114-012-0928-y
  42. Tobler I., Neuner-Jehle M. 1992. 24-h variation of vigilance in the cockroach Blaberus giganteus. Journal of Sleep Research 1 (4): 231–239. https://doi.org/10.1111/j.1365-2869.1992.tb00044.x
  43. Vinberg F., Kolesnikov A. V., Kefalov V. J. 2014. Ex vivo ERG analysis of photoreceptors using an in vivo ERG system. Vision Research 101: 108–117. https://doi.org/10.1016/j.visres.2014.06.003
  44. Yukizane M., Tomioka K. 1995. Neural pathways involved in mutual interactions between optic lobe circadian pacemakers in the cricket Gryllus bimaculatus. Journal of Comparative Physiology A 176: 601–610. https://doi.org/10.1007/BF01021580

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2025 Russian Academy of Sciences