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Interspecific variation in photoperiodic effect on the rate of preimaginal development in Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae)

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Abstract

The effects of day length on preimaginal development and reproductive maturation of females of laboratory strains which originated from two native: Irkutsk (Siberia, Russia) and Daegu (South Korea) and two invasive: Sochi (Caucasus, Russia) and Pardubice (Czechia) populations of Harmonia axyridis were investigated under the laboratory conditions. In all the 4 strains, the acceleration of development caused by the short day (all other conditions being equal) was relatively stronger in those larvae that later, at the adult stage, delayed reproductive maturation. This correlation can be considered as an indirect proof that both reactions are based on the common physiological mechanism. However, comparison of the parameters of photoperiodic responses showed that although the photoperiodic effect on reproductive maturation in individuals from Sochi and Pardubice invasive populations was relatively weak, the effect of day length on the rate of their preimaginal development was even somewhat stronger than that of individuals from Irkutsk and Daegu native populations. This uncorrelated interpopulation variation of the quantitative and qualitative photoperiodic responses suggests that in spite of the common physiological mechanism, the responses influencing preimaginal development and reproductive maturation of H. axyridis are to a certain extent independent and thus the evolution of their parameters (in particular, adaptation to new climate conditions) occurs independently.

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References

  1. Akhmedov, R.M., “Dependence of the Larval Development Duration of Different Populations of the Heart and Dart Moth (Agrotis exclamationis L.) on Temperature and Light Conditions,” Vestn. Zool. 1, 62–67 (1972).

    Google Scholar 

  2. Akhmedov, R.M. and Abdinbekova, A.A., “Factors Controlling Development and Diapause of the Broom Moth Mamestra genistae Bkh (Lepidoptera, Noctuidae),” Entomol. Obozr. 56(4), 713–720 (1977).

    Google Scholar 

  3. Belyakova, N.A. and Balueva, E.N., “Prospects for Use of the Polymorphous Cultures and Maleless Strains of Harmonia axyridis Pall. for Biological Plant Protection,” Inform. Bull. EPS IOBC 38, 35–39 (2007).

    Google Scholar 

  4. Belyakova, N.A. and Reznik, S.Ya., “First Record of the Harlequin Ladybird, Harmonia axyridis, in the Caucasus,” Europ. J. Entomol. 110(4), 699–702 (2013).

    Article  Google Scholar 

  5. Berkvens, N., Bonte, J., Berkvens, D., Tirry, L., and De Clercq, P., “Influence of Diet and Photoperiod on Development and Reproduction of European Populations of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae),” BioControl 53(1), 211–221 (2008).

    Article  Google Scholar 

  6. Bobinskaya, S.G., “The Influence of the Ecological Conditions on the Life Cycle of Hadena sordia Bkh.,” Zool. Zh. 45(11), 1659–1665 (1966).

    Google Scholar 

  7. Bradshaw, W.E. and Lounibos, L.P., “Photoperiodic Control of Development in the Pitcher-Plant Mosquito, Wyeomyia smithii,” Canad. J. Zool. 50(6), 713–719 (1972).

    Article  Google Scholar 

  8. Brown, P.M.J., Thomas, C.E., Lombaert, E., Jeffries, D.L., Estoup, A., and Handley, L.-J.L., “The Global Spread of Harmonia axyridis (Coleoptera: Coccinellidae): Distribution, Dispersal and Routes of Invasion,” BioControl 56(4), 623–641 (2011).

    Article  Google Scholar 

  9. Chernyshev, V.B., Insect Ecology (Izd-vo MGU, Moscow, 1996) [in Russian].

    Google Scholar 

  10. Clark, S.H. and Platt, A.P., “Influence of Photoperiod on Development and Larval Diapause in the Viceroy Butterfly Limenitis archippus,” J. Insect Physiol. 15(10), 1951–1957 (1969).

    Article  Google Scholar 

  11. Danilevsky, A.S., Photoperiodism and Seasonal Development of Insects (Oliver and Boyd, Edinburgh, 1965).

    Google Scholar 

  12. Danks, H.V., “The Elements of Seasonal Adaptations in Insects,” Canad. Entomol. 139(1), 1–44 (2007).

    Article  Google Scholar 

  13. Denlinger, D.L., “Induction and Termination of Pupal Diapause in Sarcophaga (Diptera: Sarcophagidae),” Biol. Bull. 142(1), 11–24 (1972).

    Article  Google Scholar 

  14. Denlinger, D.L., “Regulation of Diapause,” Annu. Rev. Entomol. 47, 93–122 (2002).

    Article  CAS  PubMed  Google Scholar 

  15. Deseó, K.V. and Sáringer, G.Y., “Photoperiodic Effect on Fecundity of Laspeyresia pomonella, Grapholitha punebrana, and G. molesta: the Sensitive Period,” Entomol. Exp. Appl. 18(2), 187–193 (1975).

    Article  Google Scholar 

  16. Doležal, P., Habuštová, O., and Sehnal, F., “Effects of Photoperiod and Temperature on the Rate of Larval Development, Food Conversion Efficiency, and Imaginal Diapause in Leptinotarsa decemlineata,” J. Insect Physiol. 53(8), 849–857 (2007).

    Article  PubMed  Google Scholar 

  17. Goryshin, N.I. and Akhmedov, R.M., “Photoperiod and Temperature as Factors of Development of the Noctuid Agrotis ypsilon (Lepidoptera, Noctuidae),” Zool. Zh. 50(1), 56–66 (1971).

    Google Scholar 

  18. Goto, S.G., “Roles of Circadian Clock Genes in Insect Photoperiodism,” Entomol. Sci. 16(1), 1–16 (2013).

    Article  Google Scholar 

  19. Gotthard, K., “Life History Plasticity in the Satyrine Butterfly Lasiommata petropolitana: Investigating an Adaptive Reaction Norm,” J. Evol. Biol. 11(1), 21–39 (1998).

    Article  Google Scholar 

  20. Hodek, I., “Diapause/Dormancy” in Ecology and Behaviour of the Ladybird Beetles (Blackwell Publishing, Chichester, UK, 2012), pp 275–342.

    Chapter  Google Scholar 

  21. Honěk, A., “Regulation of Diapause, Number of Instars, and Body Growth in the Moth Species Amathes c-nigrum (Lepidoptera: Noctuidae),” Entomol. Gen. 5(3), 221–229 (1979).

    Google Scholar 

  22. Ismail, S. and Fuzeau-Braesch, S., “Programmation de la Diapause chez Gryllus campestris,” J. Insect Physiol. 22(1), 133–139 (1976).

    Article  Google Scholar 

  23. Kamm, J.A., “Photoperiodic Regulation of Growth in an Insect: Response to Progressive Changes in Daylength,” J. Insect Physiol. 18(9), 1745–1749 (1972).

    Article  Google Scholar 

  24. Kim, N., Hong, S.J., Seol, K.Y., and Kim, S.H., “Short Daylengths Accelerate Nymphal Development of the Emma Field Cricket, Teleogryllus emma (Orthoptera: Gryllidae),” J. Asia-Pacif. Entomol. 11(1), 13–15 (2008).

    Article  Google Scholar 

  25. Kipyatkov, V.E. and Lopatina, E.B., “Intraspecific Variation of Thermal Reaction Norms for Development in Insects: New Approaches and Prospects,” Entomol. Obozr. 89(1), 33–61 (2010) [Entomol. Rev. 90 (2), 163–184 (2010)]

    Google Scholar 

  26. Koch, R.L., “The Multicolored Asian Lady Beetle, Harmonia axyridis: A Review of its Biology, Uses in Biological Control, and Non-Target Impacts,” J. Insect Sci. 3(32), 1–16 (2003).

    Article  Google Scholar 

  27. Koch, R.L. and Galvan, T.L., “Bad Side of a Good Beetle: the North American Experience with Harmonia axyridis,” BioControl 53(1), 23–35 (2008).

    Article  Google Scholar 

  28. Koštál, V. and Shimada, K., “Malfunction of Circadian Clock in the Non-Photoperiodic-Diapause Mutants of the Drosophilid Fly, Chymomyza costata,” J. Insect Physiol. 47(11), 1269–1274 (2001).

    Article  PubMed  Google Scholar 

  29. Kutcherov, D.A. and Kipyatkov, V.E., “Control of Preimaginal Development by Photoperiod and Temperature in the Dock Leaf Beetle Gastrophysa viridula (De Geer) (Coleoptera, Chrysomelidae),” Entomol. Obozr. 90(2), 249–271 (2011) [Entomol. Rev. 91 (6), 692–708 (2011)].

    Google Scholar 

  30. Kutcherov, D.A., Lopatina, E.B., and Kipyatkov, V.E., ”Photoperiod Modifies Thermal Reaction Norms for Growth and Development in the Red Poplar Leaf Beetle Chrysomela populi (Coleoptera: Chrysomelidae),” J. Insect Physiol. 57(7), 892–898 (2011).

    Article  CAS  PubMed  Google Scholar 

  31. Leimar, O., “Life History Plasticity: Influence of Photoperiod on Growth and Development in the Common Blue Butterfly,” Oikos 76(2), 228–234 (1996).

    Article  Google Scholar 

  32. Lopatina, E.B., Balashov, S.V., Kipyatkov, V.E., “First Demonstration of the Influence of Photoperiod on the Thermal Requirements for Development in Insects and in Particular the Linden-Bug, Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae),” Europ. J. Entomol. 104(1), 23–31 (2007).

    Article  Google Scholar 

  33. Lopatina, E.B., Kipyatkov, V.E., Balashov, S.V., and Kutcherov, D.A., “Photoperiod -Temperature Interaction — a New Form of Seasonal Control of Growth and Development in Insects and, in particular, in the Carabid Beetle, Amara communis (Coleoptera: Carabidae),” Zhurn. Evol. Biokhim. Fisiol. 47(6), 491–503 (2011) [J. Evol. Biochem. Physiol. 47 (6), 578–592 (2011)].

    CAS  Google Scholar 

  34. Meuti, M.E. and Denlinger, D.L., “Evolutionary Links between Circadian Clocks and Photoperiodic Diapause in Insects,” Integr. Comp. Biol. 53(1), 131–143 (2013).

    Article  PubMed Central  PubMed  Google Scholar 

  35. Musolin, D.L. and Saulich, A.K., “Photoperiodic Control of Nymphal Growth in True Bugs (Heteroptera),” Zool. Zh. 76(5), 530–542 (1997) [Entomol. Rev. 77 (6), 768–780 (1997)].

    Google Scholar 

  36. Musolin, D.L., Tsytsulina, K., and Ito, K., “Photoperiodic and Temperature Control of Reproductive Diapause Induction in the Predatory Bug Orius strigicollis (Heteroptera: Anthocoridae) and Its Implications for Biological Control,” Biol. Contr. 31(1), 91–98 (2004).

    Article  Google Scholar 

  37. Nakamura, K., “Effect of Photoperiod on the Size-Temperature Relationship in a Pentatomid Bug, Dolycoris baccarum,” J. Thermal Biol. 27(6), 541–546 (2002).

    Article  Google Scholar 

  38. Nedved, O. and Honěk, A., “Life History and Development,” in Ecology and Behaviour of the Ladybird Beetles (Blackwell Publishing, Chichester, UK, 2012), pp. 54–109.

    Chapter  Google Scholar 

  39. Nylin, S. and Gotthard, K., “Plasticity in Life-History Traits,” Annu. Rev. Entomol. 43, 63–83 (1998).

    Article  CAS  PubMed  Google Scholar 

  40. Nylin, S., Wickman, P.E.R.O., and Wiklund, C., “Life-Cycle Regulation and Life History Plasticity in the Speckled Wood Butterfly: are Reaction Norms Predictable?” Biol. J. Linn. Soc. 55(2), 143–157 (1995).

    Article  Google Scholar 

  41. Ongagna, P. and Iperti, G., “Influence of Temperature and Photoperiod on Harmonia axyridis Pall. (Col., Coccinellidae): Rapidly Obtaining Fecund Adults or in Dormancy,” J. Appl. Entomol. 117(3), 314–317 (1994).

    Article  Google Scholar 

  42. Orlova-Bienkowskaja, M.Ya., “A Dangerous Invasive Lady Beetle Harmonia axyridis (Pallas, 1773) (Coleoptera, Coccinellidae) in European Russia,” Ross. Zh. Biol. Invas. 1, 75–81 (2013).

    Google Scholar 

  43. Pegoraro, M., Gesto, J.S., Kyriacou, C.P., and Tauber, E., “Role for Circadian Clock Genes in Seasonal Timing: Testing the Bünning Hypothesis,” PLoS Genetics 10(9), e1004603 (2014).

    Article  PubMed Central  PubMed  Google Scholar 

  44. Reznik, S.Ya., “On the Effects of Diet and Photoperiod on Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae) Larval Development,” Entomol. Obozr. 89(2), 273–278 (2010) [Entomol. Rev., 90 (4), 411–414 (2010)].

    Google Scholar 

  45. Reznik, S.Ya. and Belyakova, N.A., “Photoperiodic Effects on Development and Maturation in the Invasive European Population of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae),” Trudy Russ. Entomol. Ova 84(2), 107–113 (2013).

    Google Scholar 

  46. Reznik, S.Ya. and Vaghina, N.P., “Photoperiodic Control of Development and Reproduction in Harmonia axyridis (Coleoptera: Coccinellidae),” Europ. J. Entomol. 108(3), 385–390 (2011).

    Article  Google Scholar 

  47. Reznik, S.Ya. and Vaghina, N.P., “Effects of Photoperiod and Diet on Diapause Tendency, Maturation and Fecundity in Harmonia axyridis (Coleoptera: Coccinellidae),” J. Appl. Entomol. 137(6), 452–461 (2013).

    Article  Google Scholar 

  48. Reznik, S.Ya., Dolgovskaya, M.Yu., Ovchinnikov, A.N., and Belyakova, N.A., “Weak Photoperiodic Response Facilitates the Biological Invasion of the Harlequin Ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae),” J. Appl. Entomol., DOI: 10.1111/jen.12158 (2014).

    Google Scholar 

  49. Roy, H.E. and Wajnberg, E., “From Biological Control to Invasion: the Ladybird Harmonia axyridis as a Model Species,” BioControl 53(1), 1–4 (2008).

    Article  Google Scholar 

  50. Salminen, T.S., Vesala, L., and Hoikkala, A., “Photoperiodic Regulation of Life-History Traits before and after Eclosion: Egg-to-Adult Development Time, Juvenile Body Mass and Reproductive Diapause in Drosophila montana,” J. Insect Physiol. 58(12), 1541–1547 (2012).

    Article  CAS  PubMed  Google Scholar 

  51. Saulich, A.Kh. and Musolin, D.L., “Univoltinism and its Regulation in some Temperate True Bugs (Heteroptera),” Europ. J. Entomol. 93(3), 507–518 (1996).

    Google Scholar 

  52. Saulich, A.H. and Musolin, D.L., “Four Seasons: Diversity of Seasonal Adaptations and Ecological Mechanisms Controlling Seasonal Development in True Bugs (Heteroptera) in the Temperate Climate,” Proc. Biol. Inst. St. Petersburg State Univ. 53, 25–106 (2007).

    Google Scholar 

  53. Saulich, A.Kh. and Musolin, D.L., “Diapause in the Seasonal Cycle of Stink Bugs (Heteroptera, Pentatomidae) from the Temperate Zone,” Entomol. Obozr. 90(4), 740–744 (2011) [Entomol. Rev. 92 (1), 1–26 (2012)].

    Google Scholar 

  54. Saulich, A.Kh. and Volkovich, T.A., Ecology of Photoperiodism in Insects (Izd. SPbGU, St. Petersburg, 2004) [in Russian].

    Google Scholar 

  55. Saunders, D.S., “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(5), 399–405 (1983).

    Article  Google Scholar 

  56. Saunders, D.S., Steel, C.G.H., Vafopoulou, X., and Lewis, R.D., Insect Clocks (Elsevier, Amsterdam, 2002).

    Google Scholar 

  57. Stekol’nikov, A.A., “Scientific and Pedagogical Activity of Professor Viktor Petrovich Tyshchenko (1937–1986),” Proc. Biol. Inst. St. Petersburg State Univ. 53, 3–24 (2007).

    Google Scholar 

  58. Tauber, M.J., Tauber, C.A., and Masaki, S., Seasonal Adaptations of Insects (Oxford Univ., New York, 1986).

    Google Scholar 

  59. Tyshchenko, V.P., Physiology of Insect Photoperiodism (Trudy Vses. Entomol. O-va 59),” (Nauka, Leningrad, 1977) [in Russian].

    Google Scholar 

  60. Tyshchenko, V.P., “The Signal and Vital Action of Ecological Factors,” Zh. Obshch. Biol. 41(5), 655–667 (1980).

    Google Scholar 

  61. Tyshchenko, V.P. and Gasanov, O.G., “Comparative Investigation of the Photoperiodic Regulation of Diapause and Pupal Weight in Several Moth Species (Lepidoptera),” Zool. Zh. 62(1), 63–68 (1983).

    Google Scholar 

  62. Tyshchenko, V.P. and Tyshchenko, G.F., “Seasonal Adaptations of the spotted cutworm Graphiphora c-nigrum L. (Lepidoptera, Noctuidae),” Entomol. Obozr. 67(1), 11–19 (1988).

    Google Scholar 

  63. Tyshchenko, V.P., Lanevich, V.P., and Gasanov, O.G., “Correlations of Quantitative and Qualitative Manifestations of Photoperiodism in the Cabbage Moth (Barathra brassicae),” Zh. Obshch. Biol. 38(2), 264–276 (1977).

    Google Scholar 

  64. Ukrainsky, A.S. and Orlova-Bienkowskaja, M.J., “Expansion of Harmonia axyridis Pallas (Coleoptera: Coccinellidae) to European Russia and Adjacent Regions,” Biol. Invas. 16(5), 1003–1008 (2014).

    Article  Google Scholar 

  65. Williams, K.D., Schmidt, P.S., and Sokolowski, M.B., “Photoperiodism in Insects: Molecular Basis and Consequences of Diapause,” in Photoperiodism: The Biological Calendar (Oxford Univ., New York, 2010), pp. 287–317.

    Google Scholar 

  66. Zaslavski, V.A., “Interrelations of Quantitative and Qualitative Reactions in Insect Photoperiodism,” Zool. Zh. 54(6), 913–921 (1975).

    Google Scholar 

  67. Zaslavski, V.A., “The Qualitative Evaluation of the Photoperiodic Information: Does it Exist,” Zh. Obshch. Biol. 40(2), 189–201 (1979).

    Google Scholar 

  68. Zaslavski, V.A., Photoperiodic and Temperature-Based Control of Insect Development (Proc. ZIN AN SSR) (Nauka, Leningrad, 1984) [in Russian].

    Google Scholar 

  69. Zaslavski, V.A., “The Diversity of Environmental Factors Controlling Insect Seasonal Development and the Possible Unity of Underlying Physiological Mechanism,” Entomol. Obozr. 75(2), 233–243 (1996).

    Google Scholar 

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Authors and Affiliations

  1. Zoological Institute, Russian Academy of Sciences, St. Petersburg, 199034, Russia

    S. Ya. Reznik, A. N. Ovchinnikov & M. Yu. Dolgovskaya

  2. All-Russian Institute of Plant Protection, Russian Academy of Agriculture, St. Petersburg, 196608, Russia

    N. A. Belyakova

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  1. S. Ya. Reznik
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  2. A. N. Ovchinnikov
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  3. M. Yu. Dolgovskaya
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  4. N. A. Belyakova
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Original Russian Text © S.Ya. Reznik, A.N. Ovchinnikov, M.Yu. Dolgovskaya, N.A. Belyakova, 2015, published in Entomologicheskoe Obozrenie, 2015, Vol. 94, No. 1, pp. 35–52.

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Reznik, S.Y., Ovchinnikov, A.N., Dolgovskaya, M.Y. et al. Interspecific variation in photoperiodic effect on the rate of preimaginal development in Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae). Entmol. Rev. 95, 15–27 (2015). https://doi.org/10.1134/S0013873815010029

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