Skip to main content
Log in

Long life cycles in insects

  • Published:
Entomological Review Aims and scope Submit manuscript

Abstract

Long life cycles covering more than one year are known for all orders of insects. There are different mechanisms of prolongation of the life cycle: (1) slow larval development; (2) prolongation of the adult stage with several reproduction periods; (3) prolongation of diapause; (4) combination of these mechanisms in one life cycle. Lasting suboptimal conditions (such as low temperature, low quality of food or instability of food resources, natural enemies, etc.) tend to prolong life cycles of all individuals in a population. In this case, the larvae feed and develop for longer than a year, and the active periods are interrupted by dormancy periods. The nature of this dormancy is unknown: in some cases it appears to be simple quiescence, in others it has been experimentally shown to be a true diapause. Induction and termination of these repeated dormancy states are controlled by different environmental cues, the day-length being the principal one as in the case of the annual diapause. The long life cycles resulting from prolonged adult lifespan were experimentally studied mainly in beetles and true bugs. The possibility of repeated diapause and several periods of reproductive activity is related to the fact that the adults remain sensitive to day length, which is the main environmental cue controlling their alternative physiological states (reproduction vs. diapause). Habitats with unpredictable environmental changes stimulate some individuals in a population to extend their life cycles by prolonged diapause. The properties of this diapause are poorly understood, but results of studies of a few species suggest that this physiological state differs from the true annual diapause in deeper suppression of metabolism. Induction and intensity of prolonged diapause in some species appear to be genetically controlled, so that the duration of prolonged diapause varies among individuals in a group, even that of sibles reared under identical conditions. Thus, long life cycles are realized due to the ability of insects to interrupt activity repeatedly and enter dormancy. This provides high resistance to various environmental factors. Regardless of the nature of this dormancy (quiescence, annual or prolonged diapause, or other forms) and the life cycle duration, the adults always appear synchronously after dormancy in the nature. The only feasible explanation of this is the presence of a special synchronizing mechanism, most likely both exo- and endogenous, since the adults appear not only synchronously but also in the period best suited for reproduction. As a whole, the long life cycles resulting from various structural modifications of the annual life cycle, are typical of the species living under stable suboptimal conditions when the pressure of individual environmental factors is close to the tolerance limits of the species, even though it represents its norm of existence. Such life cycles are also typical of the insects living in unstable environments with unpredictable variability of conditions, those developing in cones and galls, feeding on flowers, seeds, or fruits with limited periods of availability, those associated with the plant species with irregular patterns of blossoming and fruiting, and those consuming low-quality food or depending on unpredictable food sources (e.g., predators or parasites). Long cycles are more common in: (1) insect species at high latitudes and mountain landscapes where the vegetation season is short and unstable; (2) species living in deserts or arid areas where precipitation is unstable and often insufficient for survival of food plants; (3) inhabitants of cold and temporary water bodies that are not filled with water every year. At the same time, long life cycles sometimes occur in insects from other climatic zones as well. It is also important to note that while there is a large body of literature dealing with the long life cycles in insects, it mostly focuses on external aspects of the phenomenon. Experimental studies are needed to understand this phenomenon, first of all the nature of dormancy and mechanisms of synchronization of adult emergence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Addison, J.A., “Population Dynamics and Biology of Collembola on Truelove Lowland,” in Truelove Lowland, Devon Islands, Canada: A High Arctic Ecosystem, Ed. by L.C. Bliss (Univ. of Alberta Press, Edmonton, 1977), pp. 363–382.

    Google Scholar 

  2. Austara, Q., “Prolonged Diapause in Neodiprion sertifer Geoff. from Gaupne in Western Norway,” Medd. Norsk. Skogsfors. 27, 205–213 (1969).

    Google Scholar 

  3. Beck, S.D., “Growth and Regression in Larvae of Trogoderma glabrum (Coleoptera: Dermestidae). 1. Development Characteristics and Adaptive Functions,” Ann. Entomol. Soc. Am. 66(4), 895–900 (1971).

    Google Scholar 

  4. Benedek, P., “Revision of the Families Reduviidae and Phymatidae in the Carpathian Basin with Description of a New Species from Hungary (Heteroptera),” Rovart. Kozl. 21(2), 297–316 (1968).

    Google Scholar 

  5. Biever, K.D. and Chauvin, R.L., “Prolonged Dormancy in a Pacific Northwest Population of the Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae),” Can. Entomol. 122, 175–177 (1990).

    Article  Google Scholar 

  6. Burn, A.J., “Feeding and Growth in the Antarctic Collembolan Cryptopygus antarcticus,” Oikos 36, 59–64 (1981).

    Article  Google Scholar 

  7. Butler, E.A., Biology of the British Hemiptera-Heteroptera (London, 1923).

  8. Butler, M.G., “A 7-Year Life Cycle for Two Chironomus Species in Arctic Alaskan Tundra Ponds (Diptera: Chironomidae),” Can. J. Zool. 60, 58–60 (1982).

    Article  Google Scholar 

  9. Butler, M.G. and Anderson, D.H., “Cohort Structure, Biomass, and Production of Merovoltine Chironomus Population in a Wisconsin Bog Lake,” J. North Amer. Benthol. Soc. 9, 180–192 (1990).

    Article  Google Scholar 

  10. Chernov, Yu.I., Structure of the Subarctic Fauna (Nauka, Moscow, 1978) [in Russian].

    Google Scholar 

  11. Chernov, Yu.I. and Savchenko, E.N., “Ecology and Preimaginal Development of the Arctic Crane Fly Tipula (Pterelachisus) carinifrons Holm. (Diptera, Tipulidae),” Zool. Zh. 44(6), 777–779 (1965).

    Google Scholar 

  12. Clegg, J.S., “Cryptobiosis—A Peculiar State of Biological Organization,” Comp. Biochem. Physiol. B 128, 613–624 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Corbet, P.S., “Environmental Factors Influencing the Induction and Termination of Diapause in the Emperor Dragonfly, Anax imperator Leach (Odonata; Aeshnidae),” J. Exp. Biol. 33(1), 1–14 (1956).

    Google Scholar 

  14. Danks, H.V., “Overwintering of Some North Temperate and Arctic Chironomidae. II. Chironomid Biology,” Can. Entomol. 103(12), 1875–1910 (1971).

    Article  Google Scholar 

  15. Danks, H.V., Arctic Arthropods. A Review of Systematics and Ecology with Particular Reference to the North American Fauna (Entomol. Soc. Can., Ottawa, 1981).

    Google Scholar 

  16. Danks, H.V., Insect Dormancy: an Ecological Perspective (Biol. Survey of Canada, Ottawa, 1987).

    Google Scholar 

  17. Danks, H.V., “Long Life Cycles in Insects,” Can. Entomol. 134, 167–187 (1992).

    Google Scholar 

  18. Danks, H.V., “Seasonal Adaptations in Arctic Insects,” Integr. Comp. Biol. 44, 85–94 (2004).

    Article  Google Scholar 

  19. Danks, H.V., “Insect Adaptations to Cold and Changing Environments,” Can. Entomol. 138, 1–23 (2006).

    Article  Google Scholar 

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

    Article  Google Scholar 

  21. Danks, H.V., “Aquatic Insect Adaptations to Winter Cold and Ice,” in Aquatic Insects: Challenges to Populations. Proc. of the Royal Entomol. Society’s 24th Symp., 2007, Ed. by J. Lancaster and R.A. Briers (2008), pp. 1–19.

  22. Danks, H.V. and Lloyd, M., “The Habitats of 17-Year Periodical Cicadas (Homoptera: Cicadidae: Magicicada spp.),” Ecol. Monogr. 44, 279–324 (1974).

    Article  Google Scholar 

  23. Fal’kovich, M.I., “Seasonal Development of Desert Lepidoptera in Central Asia and Its Historical and Faunistic Analysis,” Entomol. Obozr. 58(2), 260–281 (1979).

    Google Scholar 

  24. Ferenz, H.J., “Two-Step Photoperiodic and Hormonal Control of Reproduction in the Female Beetle, Pterostichus nigrita,” J. Insect Physiol. 23(6), 671–676 (1977).

    Article  CAS  Google Scholar 

  25. Furunishi, S. and Masaki, S., “Photoperiodic Response of the Univoltine Ant-Lion Myrmeleon formicarius (Neuroptera, Myrmeleontidae),” Kontyu 9(4), 653–667 (1981).

    Google Scholar 

  26. Furunishi, S. and Masaki, S., “Seasonal Life Cycle in Two Species of Ant-Lion (Neuroptera: Myrmeleontidae),” Jap. J. Ecol. 32, 7–13 (1982).

    Google Scholar 

  27. Furunishi, S. and Masaki, S., “Photoperiodic Control of Development in the Ant-Lion Hagenomyia micans (Neuroptera: Myrmeleontidae),” Entomol. Gener. 9(1–2), 51–62 (1983).

    Google Scholar 

  28. Geispits, K.F., “Response of Univoltine Lepidoptera to Day Length,” Entomol. Obozr. 33, 17–31 (1953).

    Google Scholar 

  29. Geispits, K.F., “Photoperiodic and Temperature Reactions Determining the Seasonal Development in the Lappets Dendrolimus pini L. and D. sibiricus Tschetw. (Lepidoptera, Lasiocampidae),” Entomol. Obozr. 44(3), 538–553 (1965).

    Google Scholar 

  30. Grant, P.R., “The Priming of Periodical Cicada Life Cycles,” Trends Ecol. Evol. 20(4), 169–174 (2005).

    Article  PubMed  Google Scholar 

  31. Hanski, I., “Four Kinds of Extra Long Diapause in Insects: A Review of Theory and Observations,” Ann. Zool. Fenn. 25, 37–53 (1988).

    Google Scholar 

  32. Harz, K., “Ein Beitrag zur Biologie von Reduvius personatus L.,” Nachrichtenbl. Bayer Entomol. 1(10), 73–75 (1952).

    Google Scholar 

  33. Hasizume, H. and Numata, H., “Effects of Temperature and Photoperiod on Reproduction in the Giant Water Bug, Lethocerus deyrollei (Vuillefroy) (Heteroptera: Belostomatidae),” Japan. J. Entomol. 65(1), 55–61 (1997).

    Google Scholar 

  34. Hedlin, A.F., Miller, G.E., and Ruth, D.S., “Induction of Prolonged Diapause in Barbara colfaxiana (Lepidoptera: Olethreutidae): Correlations with Cone Crops and Weather,” Can. Entomol. 114(6), 465–471 (1982).

    Article  Google Scholar 

  35. Higaki, M., “Repeated Cycles of Chilling and Warming Effectively Terminate Prolonged Larval Diapause in the Chestnut Weevil, Curculio sikkimensis,” J. Insect Physiol. 52(5), 514–519 (2006).

    Article  CAS  PubMed  Google Scholar 

  36. Higaki, M. and Ando, Y., “Effect of Temperature on the Termination of Prolonged Initial Diapause in Eobiana japonica (Bolivar) (Orthoptera: Tettigoniidae),” Entomol. Sci. 3(2), 219–226 (2000).

    Google Scholar 

  37. Hodek, I., “Photoperiodic Response in Spring in Three Pentatomidae (Heteroptera),” Acta Entomol. Bohemoslov. 74, 209–218 (1977).

    Google Scholar 

  38. Hodek, I., Iperti, G., and Rolley, F., “Activation of Hibernating Coccinella septempunctata (Coleoptera) and Perilitus coccinellae (Hymenoptera) and the Photoperiodic Response after Diapause,” Ent. Exp. Appl. 21, 275–286 (1977).

    Article  Google Scholar 

  39. Hodek, I. and Růžička, Z., “Photoperiodic Response in Relation to Diapause in Coccinella septempunctata (Coleoptera),” Acta Entomol. Bohemoslov. 76, 209–218 (1979).

    Google Scholar 

  40. Houston, W.W.K., “The Life Cycles and Age of Carabus glabratus Paykull and C. problematicus Herbst (Col., Carabidae) on Moorland in Northern England,” Ecol. Entomol. 6, 263–271 (1981).

    Article  Google Scholar 

  41. Ichiyanagi, H., “Life History of the Stream-Dwelling Bug Aphelocheirus vittatus (Heteroptera: Aphelocheiridae) in Central Japan,” Entomol. Sci. 3(4), 603–610 (2000).

    Google Scholar 

  42. Ikeda-Kikue, K. and Numata, H., “Effects of Diet, Photoperiod and Temperature on the Postdiapause Reproduction in the Cabbage Bug, Eurydema rugosa,” Entomol. Exp. Appl. 64, 31–36 (1992).

    Article  Google Scholar 

  43. Immel, R., “Biologie und Physiologie von Reduvius personatus L.,” Z. Morphol. Ökol. Tiere 44(3), 163–195 (1955).

    Article  Google Scholar 

  44. Kalberer, N.M., Turlings, T.C.J., and Rahier, M., “An Alternative Hibernation Strategy Involving Sun-Exposed ‘Hotspots,’ Dispersal by Flight, and Host Plant Finding by Olfaction in an Alpine Leaf Beetle,” Entomol. Exp. Appl. 114, 189–196 (2005).

    Article  CAS  Google Scholar 

  45. Karban, R., “Prolonged Development in Cicadas,” in The Evolution of Insect Life Cycles, Ed. by F. Taylor and R. Karban (Springer-Verlag, New York, 1986), pp. 222–235.

    Google Scholar 

  46. Katsoyannos, P., Stathas, G.J., and Kontodimas, D.C., “Phenology of Coccinella septempunctata (Col.: Coccinellidae) in Central Greece,” Entomophaga 42(3), 435–444 (1997).

    Article  Google Scholar 

  47. Kaufmann, T., “Hibernation in the Arctic Beetle Pterostichus brevicornis in Alaska,” J. Kans. Entomol. Soc. 44, 81–92 (1971).

    Google Scholar 

  48. Khruleva, O.A., “Life Cycle of the Leaf Beetle Chrysolina subsulcata (Coleoptera, Chrysomelidae) on Wrangel Island,” Zool. Zh. 73(3), 29–37 (1994).

    Google Scholar 

  49. Khruleva, O.A., “Life Cycle and Phenology of Arctic Tiger-Moth Grammia olga (Lepidoptera, Arctiidae),” in Abstracts of Papers, IV European Workshop of Invertebrate Ecophysiology. St. Petersburg, Russia, 9–15 September 2001 (St. Petersburg, 2001), p. 101.

  50. Knülle, W., “Genetic and Environmental Determinants of Hypopus Duration in the Stored-Product Mite Lepidoglyphus destructor,” Exp. Appl. Acarol. 10, 231–258 (1991).

    Article  PubMed  Google Scholar 

  51. Koštál, V., “Eco-Physiological Phases of Insect Diapause,” J. Insect Physiol. 52, 113–127 (2006).

    Article  PubMed  CAS  Google Scholar 

  52. Krajewski, S., “Biologia i rozwoj pluskwiaka Aphelocheirus aestivalis Fabr. w Rzece Grabi,” Zesz. Nauk. Univ. Lodzk. Ser. 2 21, 63–73 (1966).

    Google Scholar 

  53. Kudryasheva, I.V., Larvae of Singing Cicadas (Homoptera, Cicadidae) of the Fauna of the USSR (Nauka, Moscow, 1979) [in Russian].

    Google Scholar 

  54. Kukal, O. and Kevan, P.G., “The Influence of Parasitism on the Life History of a High Arctic Insect, Gynaephora groenlandica (Wöcke) (Lepidoptera: Lymantriidae),” Can. J. Entomol. 65, 156–163 (1987).

    Google Scholar 

  55. Lantsov, V.I., “Specific Adaptive Features of the Life Cycle of the Arctic Crane Fly Tipula carinifrons (Diptera, Tipulidae),” Ekologiya, No. 1, 71–76 (1982).

  56. Lloyd, M. and Dybas, H.S., “The Periodical Cicada Problem. I. Population Ecology,” Evolution 20, 133–149 (1966a).

    Article  Google Scholar 

  57. Lloyd, M. and Dybas, H.S., “The Periodical Cicada Problem. II. Evolution,” Evolution 20, 466–505 (1966b).

    Article  Google Scholar 

  58. Long, C.A., “Evolution in Periodical Cicadas: A Genetical Explanation,” Evol. Theory 10(4), 209–220 (1993).

    Google Scholar 

  59. Lutz, P.E. and Jenner, Ch.E., “Life-History and Photoperiodic Responses of Nymphs of Tetragoneuria cynosura (Say),” Biol. Bull. 127(2), 304–316 (1964).

    Article  Google Scholar 

  60. Marshall, D.C., “Periodical Cicada (Homoptera: Cicadidae). Life-Cycle Variations, the Historical Emergence Record, and the Geographic Stability of Brood Distributions,” Ann. Entomol. Soc. Amer. 94(3), 386–399 (2001).

    Article  Google Scholar 

  61. Marshall, D.C. and Cooley, J.R., “Reproductive Character Displacement and Speciation in Periodical Cicadas, with Description of a New Species, 13-Year Magicicada neotredecim,” Evolution 54, 1313–1325 (2000).

    CAS  PubMed  Google Scholar 

  62. Matalin, A.V., “The Polyvariant Life Cycle of Harpalus (s. str.) affinis Schrank and Its Adaptive Significance,” Izv. Ross. Akad. Nauk Ser. Biol., No. 4, 496–505 (1998).

  63. Matalin, A.V., “Geographic Variability of the Life Cycle in Pterostichus melanarius (Coleoptera, Carabidae),” Zool. Zh. 85(5), 573–585 (2006) [Entomol. Rev. 86 (4), 909–922 (2006)].

    Google Scholar 

  64. Matalin, A.V., “Typology of Life Cycles of Ground Beetles (Coleoptera, Carabidae) in Western Palaearctic,” Zool. Zh. 86(10), 1196–1220 (2007) [Entomol. Rev. 87 (8), 947–972 (2007)].

    Google Scholar 

  65. Matalin, A.V., “Evolution of Biennial Life cycles in Ground Beetles (Coleoptera, Carabidae) of the Western Palaearctic,” in Back to the Roots and Back to the Future. Towards a New Synthesis amongst Taxonomic, Ecological and Biogeographical Approaches in Carabidology: Proc. XIII European Carabidologists Meeting, Blagoevgrad, August 20–24, 2007, Ed. by L. Penev, T. Ervin, and T. Assmann (Pensoft Publ., Sofia, 2008), pp. 259–284.

    Google Scholar 

  66. Matsuo, Y., “Cost of Prolonged Diapause and Its Relationship to Body Size in a Seed Predator,” Funct. Ecol. 20, 300–306 (2006).

    Article  Google Scholar 

  67. Minder, I.F., “Prolonged Diapause in the European Pine Sawfly,” Zool. Zh. 52(11), 1661–1670 (1973).

    Google Scholar 

  68. Morimoto, N. and Nakamura, G., “Studies on the Alpine Form of the European Pine Sawfly, Neodiprion sertifer Geoffroy (Hym.: Diprionidae) in the Central Japanese Alps. 1. The Life Cycle and the Mortality Process of Egg and Larval Stages,” Appl. Entomol. Zool. 24, 358–371 (1989).

    Google Scholar 

  69. Musolin, D.L. and Maisov, A.V., “Perception of Photoperiodic Information during Diapause Induction and Termination in the Shield Bug Graphosoma lineatum L. (Heteroptera, Pentatomidae),” in Problems of Entomology in Russia. Proc. XI Congr. of the Russian Entomological Society, St. Petersburg, 23–26 September, 1997, Vol. 2, Ed. by V.A. Krivokhatsky (St. Petersburg, 1998), p. 44 [in Russian].

  70. Nakamura, I. and Ae, S.A., “Prolonged Pupal Diapause of Papilio alexanor: Arid Zone Adaptation Directed by Larval Host Plant,” Ann. Entomol. Soc. Amer. 70(4), 481–484 (1977).

    Google Scholar 

  71. Nakamura, K., Hodek, I., and Hodkova, M., “Recurrent Photoperiodic Response in Graphosoma lineatum (Heteroptera: Pentatomidae),” Eur. J. Entomol. 93, 519–523 (1996).

    Google Scholar 

  72. Nelemans, M.N.E., den Boer, P.J., and Spee, A., “Recruitment and Summer Diapause in the Dynamics of a Population of Nebria brevicollis (Coleoptera, Carabidae),” Oikos 56, 157–169 (1989).

    Article  Google Scholar 

  73. Nesin, A.P., “On the study of Diapause in Some Cone and Seed Pests of Coniferous Trees,” Entomol. Obozr. 63(2), 226–230 (1984).

    Google Scholar 

  74. Norling, U., “The Life History and Seasonal Regulation of Aeshna viridis Eversm. in Southern Sweden (Odonata),” Entomol. Scand. 2, 170–190 (1971).

    Google Scholar 

  75. Numata, H., “Photoperiodic Sensitivity after Diapause Termination in the Bean Bug, Riptortus clavatus Thunberg (Heteroptera: Alydidae),” Appl. Entomol. Zool. 22, 352–357 (1987).

    Google Scholar 

  76. Olechovska, M., “Life Cycle of Rhithrogena loyolaea (Navas) (Ephemeroptera, Heptageniidae) in the Stream Staryski in the Tatra Mts,” Acta Hydrobiol. 23, 69–76 (1981).

    Google Scholar 

  77. Omori, N., “Comparative Studies on the Ecology and Physiology of Common and Tropical Bed Bugs, with Special Reference to the Reactions to Temperature and Moisture,” Taiwan Igakkai J. Med. Assoc. Formosa 60, 555–729 (1941).

    Google Scholar 

  78. Papáček, M., “Small Aquatic and Ripicolous Bugs (Heteroptera: Nepomorpha) as Predators and Prey: The Question of Economic Importance,” Eur. J. Entomol. 98(1), 1–12 (2001).

    Google Scholar 

  79. Puchkov, P.V., Fauna of Ukraine. Vol. 21, Issue 5: Assassin Bugs (Naukova Dumka, Kiev, 1987) [in Russian].

    Google Scholar 

  80. Powell, J.A., “Synchronized Mass-Emergences of a Yucca Moth, Prodoxus y-inversus (Lepidoptera: Prodoxidae), after 16 and 17 Years in Diapause,” Oecologia 81, 490–493 (1989).

    Article  Google Scholar 

  81. Powell, J.A., “Longest Insect Dormancy: Yucca Moth Larvae (Lepidoptera: Prodoxidae) Metamorphose after 20, 25 and 30 Years in Diapause,” Ann. Entomol. Soc. Amer. 94, 677–680 (2001).

    Article  Google Scholar 

  82. Readio, P.A., “Dormancy in Reduvius personatus (Linnaeus),” Ann. Entomol. Soc. Amer. 24, 19–39 (1931).

    Google Scholar 

  83. Ryan, J.K. and Hergert, C.R., “Energy Budget for Gynaephora groenlandica (Homeyer) and G. rossii (Curtis) (Lepidoptera: Lymantriidae) on Truelove Lowland,” in Truelove Lowland, Devon Islands, Canada: a High Arctic Ecosystem, Ed. by L.C. Bliss (Univ. of Alberta Press, Edmonton, 1977), pp. 395–609.

    Google Scholar 

  84. Saettem, L.M., “The Life History of Aphelocheirus aestivalis Fabricius (Hemiptera) in Norway,” Arch. Hydrobiol. 106(2), 245–250 (1986).

    Google Scholar 

  85. Sahota, T.S., Ibaraki, A., and Farris, S.H., “Pharate-Adult Diapause of Barbara colfaxiana (Kft.): Differentiation of 1- and 2-Year Dormancy,” Can. Entomol. 117, 873–876 (1985).

    Article  Google Scholar 

  86. Scudder, G.G.E., “The Distribution and Life Cycle of Reduvius personatus (L.) (Hemiptera: Reduviidae) in Canada,” J. Entomol. Soc. Brit. Columbia 89, 38–42 (1992).

    Google Scholar 

  87. Shindo, J. and Masaki, S., “Photoperiodic Control of Larval Development in the Semivoltine Cockroach Periplaneta japonica (Blattidae: Dictyoptera),” Ecol. Res. 10, 1–12 (1995).

    Article  Google Scholar 

  88. Sims, S.R., “Prolonged Diapause and Pupal Survival of Papilio zelicaon Lucas (Lepidoptera: Papilionidae),” J. Lepidopterol. Soc. 37(1), 29–37 (1983).

    Google Scholar 

  89. Smith, D.N., “Prolonged Larval Development in Buprestis aurulenta L. (Coleoptera: Buprestidae). A Review with New Cases,” Can. Entomol. 94, 586–593 (1962).

    Article  Google Scholar 

  90. Sømme, L., “Anaerobiosis in Some Alpine Coleoptera,” Norsk Entomol. Tiddskr. 21, 155–158 (1974).

    Google Scholar 

  91. Sømme, L., “The Adaptation of Alpine Terrestrial Arthropods to Desiccation,” Acta Oecol. 15(1), 55–62 (1994).

    Google Scholar 

  92. Sømme, L., Invertebrates in Hot and Cold Arid Environments (Springer-Verlag, Berlin, 1995).

    Google Scholar 

  93. Sømme, L. and Block, W., “Adaptation to Alpine and Polar Environments in Insects and Other Terrestrial Arthropods,” in Insects at Low Temperature, Ed. by R.E. Lee, Jr. and D.Z. Denlinger (Chapman and Hall, New York, 1991), pp. 318–359.

    Google Scholar 

  94. Sømme, L., Davidson, R.L., and Onore, G., “Adaptations of Insects at High Altitudes of Chimborazo, Ecuador,” Eur. J. Entomol. 93, 313–318 (1996).

    Google Scholar 

  95. Sota, T., “Mortality Pattern and Age Structure in Two Carabid Populations with Different Seasonal Cycles,” Res. Popul. Ecol. Kyoto Univ. 29, 237–254 (1987).

    Article  Google Scholar 

  96. Soula, B. and Menu, F., “Extended Life Cycle in the Chestnut Weevil: Prolonged or Repeated Diapause?” Entomol. Exp. Appl. 115, 333–340 (2005).

    Article  Google Scholar 

  97. Stadnitskii, V.G., “On the Biology of the European Pine Sawfly in Leningrad Province,” in Collected Works in Forest Management, Issue 8 (Leningrad, 1964), pp. 280–293 [in Russian].

  98. Stadnitskii, V.G., “Diapause in Some Conobiont Pests of Spruce in Relation with Its Seeding,” in Studies in Forest Management (Lenizdat, Pskov, 1971), pp. 233–247 [in Russian].

    Google Scholar 

  99. Sugonyaev, E.S. and Voinovich, N.D., Adaptations of Chalcid Wasps to Parasitism on Soft Scales at Different Latitudes (KMK Press, Moscow, 2006) [in Russian].

    Google Scholar 

  100. Sullivan, C.R. and Wallace, D.R., “Photoperiodism in the Development of the European Pine Sawfly, Neodiprion sertifer (Geoff.),” Can. J. Zool. 43(2), 233–245 (1965).

    Article  CAS  PubMed  Google Scholar 

  101. Sullivan, C.R. and Wallace, D.R., “Interaction of Temperature and Photoperiod in the Induction of Prolonged Diapause in Neodiprion sertifer,” Can. Entomol. 99(8), 834–850 (1967).

    Article  Google Scholar 

  102. Sullivan, C.R. and Wallace, D.R., “Variation in the Photoperiodic Response of Neodiprion sertifer,” Can. J. Zool. 46(5), 1082–1083 (1968).

    Article  Google Scholar 

  103. Tanaka, S. and Zhu, D.-H., “Presence of Three Diapauses in a Subtropical Cockroach: Control Mechanisms and Adaptive Significance,” Physiol. Entomol. 28, 323–330 (2003).

    Article  Google Scholar 

  104. The Colorado Potato Beetle Leptinotarsa decemlineata Say (Nauka, Moscow, 1981) [in Russian].

  105. Thiele, H.U., “Die Steuerung der Jahresrhythmik von Carabiden durch exogene und endogene Faktoren,” Zool. Jb. Syst. 98(3), 341–371 (1971).

    Google Scholar 

  106. Ushatinskaya, R.S., “Superdiapause in Insects,” Zh. Obshch. Biol. 64(6), 765–777 (1983).

    Google Scholar 

  107. Ushatinskaya, R.S., Cryptic Life and Anabiosis (Nauka, Moscow, 1990) [in Russian].

    Google Scholar 

  108. Valera, F., Casas-Crivill, A., and Calero-Torralbo, M.A., “Prolonged Diapause in the Ectoparasite Carnus hemapterus (Diptera: Cyclorrhapha, Acalyptratae)-How Frequent is It in Parasites?” Parasitology 133(2), 179–186 (2006).

    Article  CAS  PubMed  Google Scholar 

  109. Vinogradova, E.B. and Bogdanova, T.P., “Reproduction and Diapause Formation in the Ragweed Leaf Beetle Zygogramma suturalis F. in Stavropol Territory,” Entomol. Obozr. 67(3), 468–478 (1988).

    Google Scholar 

  110. Volkovich, 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 of St. Petersburg State University, No. 53 (2007), pp. 234–305 [in Russian].

  111. Wang, X.-P., Xue, F.-S., Hua, A., and Ge, F., “Effects of Diapause Duration on Future Reproduction in the Cabbage Beetle, Colaphellus bowringi: Positive or Negative?” Physiol. Entomol. 31, 190–196 (2006).

    Google Scholar 

  112. Watanabe, M., “Anhydrobiosis in Invertebrates,” Appl. Entomol. Zool. 41, 15–31 (2006).

    Article  CAS  Google Scholar 

  113. West, D.A., Snellings, W.M., and Herbek, T.A., “Pupal Color Dimorphism and Its Environmental Control in Papilio polyxenes asterius Stoll (Lepidoptera: Papilionidae),” J. New York Entomol. Soc. 80, 205–211 (1972).

    Google Scholar 

  114. Williams, K.S., Smith, K.G., and Stephen, F.M., “Emergence of 13-yr Periodical Cicadas (Cicadidae: Magicicada): Phenology, Mortality, and Predator Satiation,” Ecology 74, 1143–1152 (1993).

    Article  Google Scholar 

  115. Williams, K.S. and Simon, C., “The Ecology, Behavior, and Evolution of Periodical Cicadas,” Annu. Rev. Entomol. 40, 269–295 (1995).

    Article  CAS  Google Scholar 

  116. Wipking, W. and Neumann, D., “Polymorphism in the Larval Hibernation Strategy of the Burnet Moth Zygaena trifolii,” in The Evolution of Insect Life Cycles, Ed. by F. Taylor and R. Karban (Springer-Verlag, New York, 1986), pp. 125–134.

    Google Scholar 

  117. Wipking, W. and Kurtz, J., “Genetic Variability in the Diapause Response of the Burnet Moth Zygaena trifolii (Lepidoptera: Zygaenidae),” J. Insect Physiol. 46, 127–134 (2000).

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Original Russian Text © A.Kh. Saulich, 2010, published in Entomologicheskoe Obozrenie, 2010, Vol. 89, No. 3, pp. 497–531.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saulich, A.K. Long life cycles in insects. Entmol. Rev. 90, 1127–1152 (2010). https://doi.org/10.1134/S0013873810090010

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0013873810090010

Keywords

Navigation