Entomological Review

, Volume 97, Issue 2, pp 143–157 | Cite as

Seasonal cycles of noctuid moths of the subfamily Plusiinae (Lepidoptera, Noctuidae) of the Palaearctic: Diversity and environmental control

Article
  • 17 Downloads

Abstract

Analysis of data on seasonal development of noctuid moths of the subfamily Plusiinae shows that the control of their seasonal cycles is poorly understood. At the same time, the available data demonstrate considerable diversity of the seasonal patterns of Plusiinae species from different regions. The homodynamic type of seasonal development has been found in Trichoplusia ni and Ctenoplusia agnata of the tribe Argyrogrammatini and in Autographa gamma of the Plusiini. The seasonal development of these southern noctuids is accompanied by regular interzonal migrations of flying adults. When spreading northwards, they can produce a different number of annual generations, depending on the local climatic conditions, and establish temporary local populations whose longevity is limited by the available thermal resources. Adults of some species may fly back southwards, but it is more likely that individuals from temporary local populations cannot survive long winters and are destined to die. The heterodynamic type of seasonal cycles allows insects to survive in the regions with pronounced seasonality of climate. This type of seasonal development includes univoltine, multivoltine, and semivoltine seasonal cycles. Univoltine seasonal cycles with obligate diapause are known in Autographa buraetica, A. excelsa, and Syngrapha ain (Plusiini). Diapause provides tolerance to both low temperatures and a prolonged period when food is unavailable. In Syngrapha ottolenguii (Plusiini), the same result is achieved by inclusion of two photoperiodically controlled diapauses (winter larval and summer adult ones) into the life cycle. The semivoltine seasonal cycle has been reported in only one species of Plusiinae, namely Syngrapha devergens. Larvae of this moth overwinter twice before pupation. Multivoltinism is common in the tribe Plusiini. Depending on the latitude, different species of this tribe can produce up to four generations per year and overwinter as middle-instar larvae in the state of facultative diapause. However, the characteristics of diapause vary substantially between the species: diapause can be deep and stable (as in Diachrysia chrysitis, Plusiini) or unstable and thus not ensuring successful overwintering and steady population growth (as in Macdunnoughia confusa, Plusiini). The seasonal adaptations known in Plusiinae include migrations, winter and summer diapauses, photoperiodic control of larval growth rates, and seasonal polyphenism of larval body coloration. In general, seasonal adaptations of Plusiinae are determined by local environmental conditions and only loosely associated with the systematic position of particular taxa. Only the tribe Abrostolini stands apart from other taxa of Plusiinae: moths of this tribe differ not only in morphology but also in peculiarities of their seasonal development, because all the species of this tribe overwinter as pupae and their seasonal cycles are therefore different from those of the rest of Plusiinae.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Agroclimatic Resources of Belgorod Province (Gidrometeoizdat, Leningrad, 1972) [in Russian].Google Scholar
  2. 2.
    Belozerov, V.N., “Dormant Stages and Their Participation in Adjustment and Regulation of Life Cycles of Harvestmen (Arachnida, Opiliones),” Entomologicheskoe Obozrenie 91 (1), 180–216 (2012) [Entomological Review 92 (6), 688–714 (2012)].Google Scholar
  3. 3.
    Belozerov, V.N., “Seasonal Aspects of the Life Cycles of Pseudoscorpions (Arachnida, Pseudoscorpiones),” Entomologicheskoe Obozrenie 92 (1), 142–166 (2013) [Entomological Review 93 (5), 634–652 (2013)].Google Scholar
  4. 4.
    Berdys, H., Golden Plusia Polychrysia moneta (2016). http://www.gardensafari.net/en_picpages/polychrysia_ moneta.htm (accessed 01.06.2016).Google Scholar
  5. 5.
    Chapman, J.W., Bell, J.R., Burgin, L.E., Reynolds, D.R., Pettersson, L.B., et al., “Seasonal Migration to High Latitudes Results in Major Reproductive Benefits in an Insect,” Proceedings of the National Academy of Sciences 109, 14924–14929 (2012).CrossRefGoogle Scholar
  6. 6.
    Chapman, J.W., Drake, V.A., and Reynolds, D.R., “Recent Insights from Radar Studies of Insect Flight,” Annual Review of Entomology 56, 337–356 (2011).CrossRefPubMedGoogle Scholar
  7. 7.
    Danilevsky, A.S., Photoperiodism and Seasonal Development of Insects (Leningrad State University, Leningrad, 1961) [in Russian].Google Scholar
  8. 8.
    Danks, H.V., Insect Dormancy: An Ecological Perspective (Biological Survey of Canada, Ottawa, 1987).Google Scholar
  9. 9.
    Danks, H.V., “The Elements of Seasonal Adaptations in Insects,” Canadian Entomologist 139, 1–44 (2007).CrossRefGoogle Scholar
  10. 10.
    Denlinger, D.L., “Dormancy in Tropical Insects,” Annual Review of Entomology 31, 239–264 (1986).CrossRefPubMedGoogle Scholar
  11. 11.
    Denlinger, D.L., Yocum, G.D., and Rinehart, J.P., “Hormonal Control of Diapause,” in Insect Endocrinology, Ed. by L.I. Gilbert (Academic Press, London, 2012), pp. 430–463.CrossRefGoogle Scholar
  12. 12.
    Dingle, H., Migration: the Biology of Life on the Move (Oxford University Press, N.Y., 1996).Google Scholar
  13. 13.
    Förare, J., “The Biology of the Noctuid Moth Abrostola asclepiadis Schiff. (Lepidoptera, Noctuidae) in Sweden,” Entomologisk Tidskrift 116 (4), 179–186 (1995).Google Scholar
  14. 14.
    Goater, B., Ronkay, L., and Fibiger, M., Noctuidae Europaeae, Vol. 10: Catocalinae, Plusiinae (Entomological Press, Sorø, 2003).Google Scholar
  15. 15.
    Goryshin, N.I. and Saulich, A.Kh., “Studies of Seasonal Adaptations in Homodynamic Lepidoptera. II. Cold Tolerance and Survival at Low Above-Zero Temperatures,” Zoologicheskii Zhurnal 61 (1), 36–46 (1982).Google Scholar
  16. 16.
    Goryshin, N.I. and Saulich, A.Kh., “Studies of Seasonal Adaptations in Homodynamic Lepidoptera. III. Development under the Temperate Climate Conditions,” Zoologicheskii Zhurnal 62 (2), 222–232 (1983).Google Scholar
  17. 17.
    Goto, S.G. and Numata, H., “Insect Photoperiodism,” in Insect Molecular Biology and Ecology, Ed. by K.H. Hoffmann (CRC Press, Boca Raton, 2015), pp. 217–244.Google Scholar
  18. 18.
    Hill, J.K. and Gatehouse, A.G., “Effects of Temperature and Photoperiod on Development and Pre-Reproductive Period of the Silver Y Moth Autographa gamma (Lepidoptera: Noctuidae),” Bulletin of Entomological Research 82, 335–341 (1992a).CrossRefGoogle Scholar
  19. 19.
    Hill, J.K. and Gatehouse, A.G., “Genetic Control of the Pre-Reproductive Period in Autographa gamma (L.) (Silver Y Moth) (Lepidoptera: Noctuidae),” Heredity 69, 458–464 (1992b).CrossRefGoogle Scholar
  20. 20.
    Hill, J.K. and Gatehouse, A.G., “Phenotypic Plasticity and Geographical Variation in the Pre-Reproductive Period of Autographa gamma (Lepidoptera: Noctuidae) and Its Implications for Migration in This Species,” Ecological Entomology 18, 39–46 (1993).CrossRefGoogle Scholar
  21. 21.
    Honek, A., “Food Induced Variation in Thermal Constants of Development and Growth of Autographa gamma (Lepidoptera: Noctuidae),” European Journal of Entomology 99, 241–252 (2002).CrossRefGoogle Scholar
  22. 22.
    Johnson, C.G., Migration and Dispersal of Insects by Flight (Methuen, London, 1969).Google Scholar
  23. 23.
    Kaisila, J., “Immigration und Expansion der Lepidopteren in Finland in den Jahren 1869–1960,” Acta Entomologica Fennica 18, 1–452 (1962).Google Scholar
  24. 24.
    Kaneko, J., “Existence Ratio of the Silver Y Moth, Autographa gamma (L.) after Overwintering in a Cabbage Field at Sapporo, Japan,” Annual Report of the Society of Plant Protection of North Japan 44, 124–126 (1993).Google Scholar
  25. 25.
    Kaneko, J., “Differences in Cold-Hardiness between Silver Y-Moth, Autographa gamma (L.) and Asiatic Common Looper, A. nigrisigna (Walker),” Japanese Journal of Applied Entomology and Zoology 40, 303–308 (1996) [in Japanese].CrossRefGoogle Scholar
  26. 26.
    Kipyatkov, V.E. and Lopatina, E.B., “Seasonal Cycles and Strategies in Ants: Structure, Diversity, and Adaptive Traits,” in Strategies of Adaptations of Terrestrial Arthropods to Adverse Environmental Conditions (Proceedings of the Biological Research Institute, Vol. 53), Ed. by A.A. Stekolnikov (St. Petersburg State University, St. Petersburg, 2007), pp. 107–192 [in Russian].Google Scholar
  27. 27.
    Kitching, I.J., “Spectacles and Silver Y’s: a Synthesis of the Systematics, Cladistics and Biology of the Plusiinae (Lepidoptera: Noctuidae),” Bulletin of the British Museum (Natural History). Entomology 54, 75–261 (1987).Google Scholar
  28. 28.
    Klyuchko, Z.F., Noctuoid Moths of Ukraine (Izdatelstvo Raevskogo, Kiev, 2006) [in Ukrainian].Google Scholar
  29. 29.
    Koch, M., Wir bestimmen Schmetterlinge (Radebeul, Berlin, 1958).Google Scholar
  30. 30.
    Koch, M., “Warum wandern einige Schmetterlingsarten?” Entomologischen Abhandlungen 32, 203–211 (1965).Google Scholar
  31. 31.
    Koštál, V., “Eco-Physiological Phases of Insect Diapause,” Journal of Insect Physiology 52, 113–127 (2006).CrossRefPubMedGoogle Scholar
  32. 32.
    Lafontaine, J.D. and Poole, R.W., “25.1. Noctuoidea, Noctuidae (Part): Plusiinae,” in The Moths of America North of Mexico, Ed. by R. Dominick (Wedge Entomological Research Foundation, Washington, 1991).Google Scholar
  33. 33.
    Lafontaine, J.D. and Schmidt, B.C., “Annotated Check List of the Noctuoidea (Insecta, Lepidoptera) of North America North of Mexico,” ZooKeys 40, 1–239 (2010).CrossRefGoogle Scholar
  34. 34.
    Li, C., Fu, X., Feng, H., Ali, A., Li, C., and Wu, K., “Seasonal Migration of Ctenoplusia agnata (Lepidoptera: Noctuidae) over the Bohai Sea in Northern China,” Journal of Economic Entomology 107 (3), 1003–1008 (2014).CrossRefPubMedGoogle Scholar
  35. 35.
    Matov, A.Yu. and Kononenko, V.S., Trophic Associations of the Larvae of Noctuoid Moths in the Fauna of Russia (Lepidoptera, Noctuoidea: Nolidae, Erebidae, Euteliidae, Noctuidae) (Dalnauka, Vladivostok, 2012) [in Russian].Google Scholar
  36. 36.
    Matov, A.Yu., Kononenko, V.S., and Sviridov, A.V., “Noctuidae,” in Catalogue of the Lepidoptera of Russia, Ed. by S.Yu. Sinev (KMK Scientific Press, Moscow, 2008), pp. 239–296 [in Russian].Google Scholar
  37. 37.
    Merivee, E.E., “Criteria of Lability of Photoperiodic Response and Their Relation to Cold Tolerance in Noctuid Moths Plusia chrysitis L. and Macdunnoughia confusa Stph.,” in Cold Tolerance in Insects and Acarines: Proceedings of a Symposium, April 19–21, 1971, Ed. by V.Yu. Maavara (Tartu, 1971), pp. 79–83.Google Scholar
  38. 38.
    Merivee, E.E., Cold Tolerance in Insects (Estonian SSR Academy of Sciences, Tartu, 1978) [in Russian].Google Scholar
  39. 39.
    Merzheevskaya, O.I., Larvae of Noctuidae: Their Biology and Morphology (Nauka i Tekhnika, Minsk, 1967) [in Russian].Google Scholar
  40. 40.
    Musolin, D.L. and Saulich, A.Kh., “Photoperiodic Control of Nymphal Growth in True Bugs (Heteroptera),” Zoologicheskii Zhurnal 76 (5), 530–540 (1997) [Entomological Review 77 (6), 768–780 (1997)].Google Scholar
  41. 41.
    Musolin, D.L. and Saulich, A.Kh., “Diapause in Pentatomoidea,” in Invasive Stink Bugs and Related Species (Pentatomoidea): Biology, Higher Systematics, Semiochemistry, and Management, Ed. by J.E. McPherson (CRC Press, Boca Raton, 2017), pp. 475–542.Google Scholar
  42. 42.
    Navas, C.A., and Carvalho, J.E. (Eds.), Aestivation: Molecular and Physiological Aspects (Progress in Molecular and Subcellular Biology 49) (Springer-Verlag, Berlin-Heidelberg, 2010).Google Scholar
  43. 43.
    Nomura, M., “Allozyme Variation and Phylogenetic Analyses of Genera and Species of Japanese Plusiinae (Lepidoptera: Noctuidae),” Applied Entomology and Zoology 33 (4), 513–523 (1998).Google Scholar
  44. 44.
    Novák, I., “Hibernation of the Silver Y-Moth Autographa gamma L. (Lepidoptera: Noctuidae) under the Climatic Conditions of Central Europe,” in Proceedings of the XIII International Entomological Congress, August 2–9, 1968. Vol. 1 (Moscow, 1968), p. 533.Google Scholar
  45. 45.
    Novák, I., “Prezimovani mury gama (Autographa gamma L., Lepidoptera: Noctuidae) ve Stredni Evrope,” Ochrana Rostlin 8, 305–312 (1972).Google Scholar
  46. 46.
    Saito, O., “Notes on Larval Hibernation of the Alfalfa Looper, Autographa gamma (L.) on Cabbage Plant in Sapporo, Hokkaido,” Annual Report of the Society of Plant Protection of North Japan 39, 217 (1988).Google Scholar
  47. 47.
    Saito, O., “Diapause-Like Prolongation of Larval Duration under Short-Day Photoperiod and Low Temperature Conditions in the Silver Y Moth, Autographa gamma L. (Lepidoptera: Noctuidae),” Applied Entomology and Zoology 42 (3), 391–395 (2007).CrossRefGoogle Scholar
  48. 48.
    Saulich, A.Kh., Seasonal Development and Dispersal Potential of Insects (St. Petersburg State Univ., St. Petersburg, 1999) [in Russian].Google Scholar
  49. 49.
    Saulich, A.Kh. and Musolin, D.L., “Times of the Year: the Diversity of Seasonal Adaptations and Ecological Mechanisms Controlling Seasonal Development of True Bugs (Heteroptera) in the Temperate Climate,” in Strategies of Adaptations of Terrestrial Arthropods to Adverse Environmental Conditions (Proceedings of the Biological Research Institute, Vol. 53), Ed. by A.A. Stekolnikov (St. Petersburg State University, St. Petersburg, 2007), pp. 25–106 [in Russian].Google Scholar
  50. 50.
    Saulich, A.Kh. and Musolin, D.L., “Seasonal Cycles in Stink Bugs (Heteroptera, Pentatomidae) from the Temperate Zone: Diversity and Control,” Entomolo-gicheskoe Obozrenie 93 (2), 263–302 (2014) [Entomological Review 94 (6), 785–814 (2014)].Google Scholar
  51. 51.
    Saulich, A.Kh. and Musolin, D.L., “Seasonal Development of Plusia festucae and Its Environmental Control,” in The Kataev Memorial Readings–IX. Dendrobiotic Invertebrates and Fungi and their Role in Forest Ecosystems. Proceedings of the International Conference, Ed. by D.L. Musolin and A.V. Selikhovkin (St. Petersburg State Forest Technical University, St. Petersburg, 2016), pp. 106–107.Google Scholar
  52. 52.
    Saulich, A.Kh. and Musolin, D.L., “Seasonal Cycles of Pentatomoidea,” in Invasive Stink Bugs and Related Species (Pentatomoidea): Biology, Higher Systematics, Semiochemistry, and Management, Ed. by J.E. McPherson (CRC Press, Boca Raton, 2017), pp. 543–585.Google Scholar
  53. 53.
    Saulich, A.Kh. and Sokolova, I.V., “Seasonal Adaptations in Noctuid Moths (Lepidoptera, Noctuidae),” Entomologicheskoe Obozrenie 81 (3), 529–546 (2002) [Entomological Review 82 (9), 1127–1141 (2002)].Google Scholar
  54. 54.
    Saulich, A.Kh. and Volkovitsh, T.A., Ecology of Photoperiodism in Insects (St. Petersburg State Univ., St. Petersburg, 2004) [in Russian].Google Scholar
  55. 55.
    Saulich, A.Kh., Sokolova, I.V., and Musolin, D.L., “Seasonal Development of the Dark Spectacle Abrostola triplasia (L.) (Lepidoptera, Noctuidae) and Its Environmental Control,” Entomologicheskoe Obozrenie 94 (3), 481–488 (2015) [Entomological Review 95 (6), 687–692 (2015)].Google Scholar
  56. 56.
    Saunders, D.S. (with Steel, C.G.H., Vafopoulou, X., and Lewis, R.D.), Insect Clocks, 3rd ed. (Elsevier Science, Amsterdam, 2002).Google Scholar
  57. 57.
    Speidel, W., Faner, W., and Naumann, C.M., “Phylogeny of the Noctuidae (Lepidoptera),” Systematic Entomology 21 (3), 219–251 (1996).CrossRefGoogle Scholar
  58. 58.
    Storey, K.B. and Storey, J.M., “Aestivation: Signaling and Hypometabolism,” Journal of Experimental Biology 215 (9), 1425–1433 (2012).CrossRefPubMedGoogle Scholar
  59. 59.
    Sukhareva, I.L., “Family Noctuidae,” in Insects and Acarines as Agricultural Pests, Vol. 3: Lepidoptera, Part 2, Ed. by V.I. Kuznetsov (Nauka, St. Petersburg, 1999), pp. 332–376 [in Russian].Google Scholar
  60. 60.
    Tauber, M.J., Tauber, C.A., and Masaki, S., Seasonal Adaptations of Insects (Oxford University Press, New York, 1986).Google Scholar
  61. 61.
    Vojnits, A., “Az ‘igazi’ vándorlepkék,” Folia Entomologica Hungarica 8, 167–175 (1966).Google Scholar
  62. 62.
    Volkovitsh, T.A., “Diapause in the Life Cycles of Lacewings (Neuroptera, Chrysopidae),” in Strategies of Adaptations of Terrestrial Arthropods to Adverse Environmental Conditions (Proceedings of the Biological Research Institute, Vol. 53), Ed. by A.A. Stekolnikov (St. Petersburg State University, St. Petersburg, 2007), pp. 234–304 [in Russian].Google Scholar
  63. 63.
    Yamamura, S. and Sasaki, M., “Some Notes on Larval Development and Diagnosis in Autographa buraetica (Staudinger) (Lepidoptera: Plusiinae) in Japan,” Japan Heterocerists’ Journal 240, 269–272 (2006) [in Japanese with English summary].Google Scholar
  64. 64.
    Yamamura, S. and Sasaki, M., “Larval-Pupal Bionomics of Syngrapha ain (Hochenwarth) (Noctuidae, Plusiinae) in the Japanese Population Based on Artificial Rearing and Field Observation,” Japan Heterocerists’ Journal 248, 412–417 (2008) [in Japanese with English summary].Google Scholar
  65. 65.
    Yamamura, S., Ikarashi, M., and Sasaki, M., “A Critical Photoperiod which Induces Larval Diapause, and Observation of Its Development in Diachrysia chryson (Esper) (Noctuidae: Plusiinae),” Japan Heterocerists’ Journal 249, 434–437 (2008a) [in Japanese with English summary].Google Scholar
  66. 66.
    Yamamura, S., Ikarashi, M., and Sasaki, M., “Dual Photoperiodic Regulation to Enable Univoltine Life Cycle in Alpine Silver-Y Moth, Syngrapha ottolenguii (Noctuidae: Plusiinae) without Obligatory Diapause,” Applied Entomology and Zoology 43 (1), 105–112 (2008b).Google Scholar
  67. 67.
    Yathom, S., and Rivnay, E., “Phenology and Distribution of Phytometrinae in Israel,” Zeitschrift für Angewandte Entomologie 61 (1), 1–16 (1968).Google Scholar

Copyright information

© Pleiades Publishing, Inc. 2017

Authors and Affiliations

  • A. Kh. Saulich
    • 1
  • I. V. Sokolova
    • 2
  • D. L. Musolin
    • 3
  1. 1.St. Petersburg State UniversitySt. PetersburgRussia
  2. 2.Astrakhan State Biosphere ReserveAstrakhanRussia
  3. 3.St. Petersburg State Forest Technical UniversitySt. PetersburgRussia

Personalised recommendations