Abstract
The effects of constant temperatures (15, 20, 25, and 30°C) and thermoperiods (daily alternations of high temperature of 25 or 30°C and low temperature of 15 or 20°C) on maternal induction of diapause in the offspring of egg parasitoids Trichogramma telengai Sor. (Hymenoptera, Trichogrammatidae) was studied. Each combination of temperatures was tested in two variants: “short-day” (with the periods of high and low temperature lasting 12 h) and “long-day” (with the periods of high and low temperature lasting 18 and 6 h, respectively). In addition, constant temperatures equal to the thermoperiod means were tested. The experiments showed that thermoperiods and constant temperatures significantly influenced diapause induction in the T. telengai progeny, both in interaction with different photoperiods and under conditions of constant darkness. However, thermoperiods do not seem to convey information on day length and are unlikely to serve as seasonal cues in Trichogramma.
REFERENCES
Beck, S.D., Insect thermoperiodism, Annu. Rev. Entomol., 1983, vol. 28, no. 1, p. 91. https://www.annualreviews.org/doi/abs/10.1146/annurev.en.28.010183.000515
Beck, S.D., Thermoperiodic induction of larval diapause in the European corn borer, Ostrinia nubilalis, J. Insect Physiol., 1982, vol. 28, no. 3, p. 277. https://doi.org/10.1016/0022-1910(82)90087-7
Boivin, G., Overwintering strategies of egg parasitoids, in Biological Control with Egg Parasitoids, Wajnberg, E. and Hassan, S.A., Eds., Wallingford: CAB Int., 1994, p. 219.
Claret, J. and Carton, Y., Diapause in a tropical species, Cothonaspis boulardi (Parasitic Hymenoptera), Oecologia, 1980, vol. 45, no. 1, p. 32. https://link.springer.com/article/10.1007/BF00346703
Danilevskii, A.S., Fotoperiodizm i sezonnoe razvitie nasekomyh (Photoperiodism and Seasonal Development of Insects), Leningrad: LGU, 1961.
Danks, H.V., The elements of seasonal adaptations in insects, Can. Entomol., 2007, vol. 139, no. 1, p. 1. https://doi.org/10.4039/n06-048
Delava, E., Fleury, F., and Gibert, P., Effects of daily fluctuating temperatures on the Drosophila–Leptopilina boulardi parasitoid association, J. Therm. Biol., 2016, vol. 60, p. 95. https://doi.org/10.1016/j.jtherbio.2016.06.012
Denlinger, D.L., Insect Diapause, Cambridge: Cambridge Univ., 2022.
Denlinger, D.L., Regulation of diapause, Annu. Rev. Entomol., 2002, vol. 47, p. 93. https://doi.org/10.1146/annurev.ento.47.091201.145137
Goryshin, N.I. and Kozlova, R.N., Thermoperiodism as a factor in insect development, Zh. Obshch. Biol., 1967, vol. 28, no. 3, p. 278.
Mai Fu Kvi and Zaslavskii, V. A., Photoperiodic and temperature responses of Trichogramma euproctidis (Hymenoptera, Trichogrammatidae), Zool. Zh., 1983, vol. 62, no. 11, p. 1676.
Menaker, M. and Gross, G., Effect of fluctuating temperature on diapause induction in the pink bollworm, J. Insect Physiol., 1965, vol. 11, no. 7, p. 911. https://doi.org/10.1016/0022-1910(65)90194-0
Numata, H., Saulich, A.H., and Volkovich, T.A., Photoperiodic responses of the linden bug, Pyrrhocoris apterus, under conditions of constant temperature and under thermoperiodic conditions, Zool. Sci., 1993, vol. 10, no. 3, p. 521. https://dl.ndl.go.jp/info:ndljp/pid/10860643
Reznik, S.Ya., Ecological and evolutionary aspects of photothermic regulation of diapause in Trichogrammatidae, Zh. Evol. Biokhim. Fiziol., 2011, vol. 47, no. 6, p. 434. https://www.elibrary.ru/item.asp?id=17047001
Reznik, S.Y. and Voinovich, N.D., Diapause induction in Trichogramma telengai: the dynamics of maternal thermosensitivity, Physiol. Entomol., 2016, vol. 41, no. 4, p. 335. https://doi.org/10.1111/phen.12149
Reznik, S.Ya., Vaghina, N.P., and Voinovich, N.D., Maternal influence on diapause induction in Trichogramma (Hymenoptera, Trichogrammatidae): the dynamics of photosensitivity, J. Appl. Entomol., 2011, vol. 135, no. 6, p. 438. https://doi.org/10.1111/j.1439-0418.2010.01563.x
Reznik, S.Y., Voinovich, N.D., and Samartsev, K.G., Grandmaternal temperature effect on diapause induction in Trichogramma telengai (Hymenoptera: Trichogrammatidae), J. Insect Physiol., 2020, vol. 124, 104072. https://doi.org/10.1016/j.jinsphys.2020.104072
Rock, G.C., Thermoperiodic effects on the regulation of larval diapause in the tufted apple budworm (Lepidoptera: Tortricidae), Environ. Entomol., 1983, vol. 12, no. 5, p. 1500. https://doi.org/10.1093/ee/12.5.1500
Saulich, A.Kh. and Volkovich, T.A., Ekologiya fotoperiodizma nasekomykh (Ecology of Insect Photoperiodism), St. Petersburg: SPbGU, 2004.
Saunders, D.S., Insect photoperiodism: seasonal development on a revolving planet, Eur. J. Entomol., 2020, vol. 117, no. 1, p. 328. https://doi.org/10.14411/eje.2020.038
Saunders, D.S., Insect photoperiodism: effects of temperature on the induction of insect diapause and diverse roles for the circadian system in the photoperiodic response, Entomol. Sci., 2014, vol. 17, no. 1, p. 25. https://doi.org/10.1111/ens.12059
Saunders, D.S., Photoperiodic time measurement in Sarcophaga argyrostoma: an attempt to use daily temperature cycles to distinguish external from internal coincidence, J. Comp. Physiol. A, 1984, vol. 154, no. 6, p. 789. https://link.springer.com/article/10.1007/BF00610679
Saunders, D.S., Steel, C.G.H., Vafopoulou, X., and Lewis, R.D., Insect Clocks, Amsterdam: Elsevier, 2002.
Saunders, D.S., Thermoperiodic control of diapause in an insect: theory of internal coincidence, Science, 1973, vol. 181, no. 4097, p. 358. https://doi.org/10.1126/science.181.4097.358
Smith, S.M., Biological control with Trichogramma: advances, successes, and potential of their use, Annu. Rev. Entomol., 1996, vol. 41, p. 375. https://doi.org/10.1146/annurev.en.41.010196.002111
Sorokina, A.P., The use of Trichogramma: Past and present, Zashchita i Karantin Rastenii, 2011, vol. 10, p. 9. https://cyberleninka.ru/article/n/primenenie-trihogrammy-proshloe-i-nastoyaschee
Takano, Y., Goto, S.G., and Gotoh, T., Diapause induction in Eotetranychus smithi (Acari: Tetranychidae): effect of average temperature, but not of thermoperiod, Physiol. Entomol., 2021, vol. 46, no. 1, p. 8. https://doi.org/10.1111/phen.12335
Tauber, M.J., Tauber, C.A., and Masaki, S., Seasonal Adaptations of Insects, New York: Oxford Univ., 1986.
Vaghina, N.P., Voinovich, N.D., and Reznik, S.Ya., Maternal thermal and photoperiodic effects on the progeny diapause in Trichogramma telengai Sorokina (Hymenoptera: Trichogrammatidae), Entomol. Sci., 2014, vol. 17, no. 2, p. 198. https://doi.org/10.1111/ens.12045
Voinovich, N.D., Reznik, S.Y., and Vaghina, N.P., Maternal thermal effect on diapause in Trichogramma species (Hymenoptera: Trichogrammatidae), J. Appl. Entomol., 2015, vol. 139, no. 10, p. 783. https://doi.org/10.1111/jen.12214
Voinovich, N.D., Vaghina, N.P., and Reznik, S.Ya., Comparative analysis of maternal and grand-maternal photoperiodic responses of Trichogramma species (Hymenoptera: Trichogrammatidae), Eur. J. Entomol., 2013, vol. 110, no. 3, p. 451.
Zaslavskii, V. A., Fotoperiodicheskii i temperaturnyi kontrol razvitiya nasekomykh (Photoperiodic and Temperature Control of Insect Development), Leningrad: Nauka, 1984.
Zaslavskii, V. A. and Umarova, T. Ya., Photoperiodic and temperature control of diapause in Trichogramma evanescens Westw. (Hymenoptera, Trichogrammatidae), Entomol. Obozr., 1981, vol. 60, no. 4, p. 721.
Zaslavskii, V. A. and Umarova, T. Ya., Environmental and endogenous control of diapause in Trichogramma species, Entomophaga, 1990, vol. 35, no. 1, p. 23. https://doi.org/10.1007/BF02374297
ACKNOWLEDGMENTS
The authors are deeply grateful to T.Ya. Umarova (Zoological Institute of the Russian Academy of Sciences) for her help in the experiments.
Funding
The work was carried out as part of the state-funded project “Systematics, Morphology, Ecophysiology, and Evolution of Insects” (State Registration Number: 122031100272-3).
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Statement on the welfare of animals. All the applicable international, national, and institutional guidelines for the care and use of animals were followed. All the procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
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Voinovich, N.D., Reznik, S.Y. Thermoperiodic Effect on Diapause Induction in the Progeny of Female Trichogramma telengai Sor. (Hymenoptera, Trichogrammatidae): Adjustment but not Substitution of Photoperiodism. Entmol. Rev. 103, 1–6 (2023). https://doi.org/10.1134/S0013873823010013
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DOI: https://doi.org/10.1134/S0013873823010013