1932

Abstract

Although it is generally more adaptive for insects to produce additional generations than to have longer life cycles, some insects produce one or fewer generations per year (univoltine or semivoltine life cycles, respectively). Some insects with the potential to produce multiple generations per year produce a univoltine life cycle in response to environmental conditions. Obligatory univoltine insects have a single long diapause or multiple diapauses in different seasons. Semivoltine insects have multiple diapauses in different years, a prolonged diapause for more than a year, or diapause controlled by a circannual rhythm. Diapause in these insects greatly varies among species both in the physiological mechanism and in the evolutionary background, and there is no general rule defining it. In this review, we survey the physiological control of univoltine and semivoltine insects’ diapause and discuss the adaptive significance of the long life cycles. Although constraints such as slow development are sometimes responsible for these life cycles, the benefits of these life cycles can be explained by bet-hedging in many cases. We also discuss the effect of climate warming on these life cycles as a future area of research.

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2023-01-23
2024-10-06
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Literature Cited

  1. 1.
    Ando Y. 1983. Diapause and geographic variation in a leaf beetle. Diapause and Life Cycle Strategies in Insects, ed. VK Brown, I Hodek 127–141 The Hague: Dr. W. Junk Publ.
    [Google Scholar]
  2. 2.
    Andrewartha HG. 1943. Diapause in the eggs of Austroicetes cruciata, Sauss. (Acrididae) with particular reference to the influence of temperature on the elimination of diapause. Bull. Entomol. Res. 34:1–17
    [Google Scholar]
  3. 3.
    Andrewartha HG. 1952. Diapause in relation to the ecology of insects. Biol. Rev. 27:50–107
    [Google Scholar]
  4. 4.
    Armes NJ. 1990. The biology of Anthrenus sarnicus Mroczkowski (Coleoptera: Dermestidae): I. Egg and larval development. J. Stored Prod. Res. 26:11–22
    [Google Scholar]
  5. 5.
    Bale JS, Hayward SAL. 2010. Insect overwintering in a changing climate. J. Exp. Biol. 213:980–94
    [Google Scholar]
  6. 6.
    Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM et al. 2002. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob. Change Biol. 8:1–16
    [Google Scholar]
  7. 7.
    Blake GM. 1958. Diapause and the regulation of development in Anthrenus verbasci (L.) (Col., Dermestidae). Bull. Entomol. Res. 49:751–75
    [Google Scholar]
  8. 8.
    Butterfield J. 1976. Effect of photoperiod on a winter and on a summer diapause in two species of cranefly (Tiplidae). J. Insect Physiol. 22:1443–46
    [Google Scholar]
  9. 9.
    Chippendale GM, Yin C-M. 1973. Endocrine activity retained in diapause insect larvae. Nature 246:511–12
    [Google Scholar]
  10. 10.
    Choi WI, Park YK, Park YS, Ryoo MI, Lee HP. 2011. Changes in voltinism in a pine moth Dendrolimus spectabilis (Lepidoptera: Lasiocampidae) population: implications of climate change. Appl. Entomol. Zool. 46:319–25
    [Google Scholar]
  11. 11.
    Convey P 2010. Life-history adaptations to polar and alpine environments. Low Temperature Biology of Insects DL Denlinger, RE Lee 297–321 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  12. 12.
    Coombs CW, Woodroffe GE. 1983. The effect of temperature upon the longevity, fecundity and circannual development of Anthrenus sarnicus Mroczkowski (Coleoptera: Dermestidae). J. Stored Prod. Res. 19:111–15
    [Google Scholar]
  13. 13.
    Corbet PS. 2002. Stadia and growth ratios of Odonata: a review. Int. J. Odonatol. 5:45–73
    [Google Scholar]
  14. 14.
    Dalin P. 2011. Diapause induction and termination in a commonly univoltine leaf beetle (Phratora vulgatissima). Insect Sci 18:443–50
    [Google Scholar]
  15. 15.
    Dalin P, Nylin S. 2012. Host-plant quality adaptively affects the diapause threshold: evidence from leaf beetles in willow plantations. Ecol. Entomol. 37:490–99
    [Google Scholar]
  16. 16.
    Danilevskii AS. 1961. Photoperiodism and Seasonal Development of Insects Leningrad, USSR: Leningrad State Univ. (in Russian)
    [Google Scholar]
  17. 17.
    Danks HV. 1987. Insect Dormancy: An Ecological Perspective. Ottawa: Biol. Surv. Can.
    [Google Scholar]
  18. 18.
    Danks HV. 1992. Long life cycles in insects. Can. Entomol. 124:167–87
    [Google Scholar]
  19. 19.
    Danks HV, Oliver DR. 1972. Seasonal emergence of some high arctic Chironomidae (Diptera). Can. Entomol. 104:661–86
    [Google Scholar]
  20. 20.
    Denlinger DL 1991. Relationship between cold hardiness and diapause. Insects at Low Temperature RE Lee, DL Denlinger 174–98 New York: Chapman & Hall
    [Google Scholar]
  21. 21.
    Dewar RC, Watt AD. 1992. Predicted changes in the synchrony of larval emergence and budburst under climatic warming. Oecologia 89:557–59
    [Google Scholar]
  22. 22.
    Evans EW. 2021. Partial bivoltinism in a gregarious endoparasitoid: larval diapause as influenced by season and sharing a host. Entomol. Exp. Appl. 169:145–53
    [Google Scholar]
  23. 23.
    Forrest JR. 2016. Complex responses of insect phenology to climate change. Curr. Opin. Insect Sci. 17:49–54
    [Google Scholar]
  24. 24.
    Furunishi S, Masaki S. 1982. Seasonal life cycle in two species of ant-lion (Neuropteran: Myrmeleontidae). Jpn. J. Ecol. 32:7–13
    [Google Scholar]
  25. 25.
    Furunishi S, Masaki S. 1983. Photoperiodic control of development in the ant-lion Hagenomyia micans (Neuropteran: Myrmeleontidae). Entomol. Gen. 9:51–62
    [Google Scholar]
  26. 26.
    Gerling D, Guershon M, Erel E, Inbar M. 2011. Diapause and its regulation in the whitefly Trialeurodes lauri. Bull. Entomol. Res. 101:741–47
    [Google Scholar]
  27. 27.
    Gomi T, Takeda M. 1992. A quantitative photoperiodic response terminates summer diapause in the tailed zygaenid moth, Elcysma westwoodii. J. Insect Physiol. 38:665–70
    [Google Scholar]
  28. 28.
    Grevstad FS, Coop LB. 2015. The consequences of photoperiodism for organisms in new climates. Ecol. Appl. 25:1506–17
    [Google Scholar]
  29. 29.
    Gwinner E. 1986. Circannual Rhythms Berlin: Springer
    [Google Scholar]
  30. 30.
    Hansen EM, Bentz BJ, Turner DL. 2001. Physiological basis for flexible voltinism in the spruce beetle (Coleoptera: Scolytidae). Can. Entomol. 133:805–17
    [Google Scholar]
  31. 31.
    He XZ, Wang Q, Walker JT, Rogers DJ, Lo PL. 2010. A sophisticated life history strategy in a parasitoid wasp: producing univoltine and multivoltine phenotypes in a local population. Biol. Control 54:276–84
    [Google Scholar]
  32. 32.
    Hidaka T, Ishizuka Y, Sakagami Y 1971. Control of pupal diapause and adult differentiation in a univoltine papilionid butterfly, Luehdorfia japonica. J. Insect Physiol. 17:197–203
    [Google Scholar]
  33. 33.
    Higaki M. 2005. Effect of temperature on the termination of prolonged larval diapause in the chestnut weevil Curculio sikkimensis (Coleoptera: Curculionidae). J. Insect Physiol. 51:1352–58
    [Google Scholar]
  34. 34.
    Higaki M. 2006. Repeated cycles of chilling and warming effectively terminate prolonged larval diapause in the chestnut weevil Curculio sikkimensis. J. Insect Physiol. 52:514–19
    [Google Scholar]
  35. 35.
    Higaki M, Ando Y. 1999. Seasonal and altitudinal adaptations in three katydid species: ecological significance of initial diapause. Entomol. Sci. 2:1–11
    [Google Scholar]
  36. 36.
    Higaki M, Ando Y. 2000. Effect of temperature on the termination of prolonged initial diapause in Eobiana japonica (Bolivar) (Orthoptera: Tettigoniidae). Entomol. Sci. 3:219–26
    [Google Scholar]
  37. 37.
    Higaki M, Ihara F, Toyama M, Mishiro K. 2010. Thermal response and reversibility of prolonged larval diapause in the chestnut weevil, Curculio sikkimensis. J. Insect Physiol. 56:616–21
    [Google Scholar]
  38. 38.
    Higaki M, Toyama M. 2012. Evidence for reversible change in intensity of prolonged diapause in the chestnut weevil, Curculio sikkimensis. J. Insect Physiol. 58:56–60
    [Google Scholar]
  39. 39.
    Hodek I. 1971. Sensitivity to photoperiod in Aelia acuminata (L.) after adult diapause. Oecologia 6:152–55
    [Google Scholar]
  40. 40.
    Hodek I. 1979. Intermittent character of adult diapause in Aelia acuminata (Heteroptera). J. Insect Physiol. 25:867–71
    [Google Scholar]
  41. 41.
    Hodek I, Hodková M. 1988. Multiple role of temperature during insect diapause: a review. Entomol. Exp. Appl. 49:153–65
    [Google Scholar]
  42. 42.
    Honek A, Martinkova Z, Pekár S. 2020. How climate change affects the occurrence of a second generation in the univoltine Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). Ecol. Entomol. 45:1172–79
    [Google Scholar]
  43. 43.
    Horwath KL, Duman JG. 1983. Photoperiodic and thermal regulation of antifreeze protein levels in the beetle Dendroides canadensis. J. Insect Physiol. 29:907–17
    [Google Scholar]
  44. 44.
    Hunter MD, McNeil JN. 1997. Host-plant quality influences diapause and voltinism in a polyphagous insect herbivore. Ecology 78:977–86
    [Google Scholar]
  45. 45.
    Ichikawa M, Nishiitsutsuji-Uwo J, Yashika K. 1956. Studies on the insect metamorphosis VI. Effect of low temperature on the morphogenesis of Luehdorfia-pupae. Mem. Coll. Sci. Univ. Kyoto B 23:19–26
    [Google Scholar]
  46. 46.
    Ikeda-Kikue K, Numata H. 2001. Timing of diapause induction in the cabbage bug Eurydema rugosum (Heteroptera: Pentatomidae) on different host plants. Acta Soc. Zool. Bohem. 65:197–205
    [Google Scholar]
  47. 47.
    Ingram BR, Jenner CE. 1976. Life histories of Enallagma hageni (Walsh) and E. aspersum (Hagen) (Zygoptera: Coenagrionidae). Odonatologica 5:331–45
    [Google Scholar]
  48. 48.
    Ingrisch S. 1986. The plurennial life cycles of the European Tettigoniidae (Insecta: Orthoptera). 1. The effect of temperature on embryonic development and hatching. Oecologia 70:606–16
    [Google Scholar]
  49. 49.
    Ingrisch S. 1986. The plurennial life cycles of the European Tettigoniidae (Insecta: Orthoptera). 3. The effect of drought and the variable duration of the initial diapause. Oecologia 70:624–30
    [Google Scholar]
  50. 50.
    IPCC (Intergov. Panel Clim. Change) 2021. Climate change 2021: the physical science basis Rep., IPCC, Geneva https://www.ipcc.ch/report/sixth-assessment-report-working-group-i/
    [Google Scholar]
  51. 51.
    Ishihara M. 1999. Adaptive phenotypic plasticity and its difference between univoltine and multivoltine populations in a bruchid beetle, Kytorhinus sharpianus. Evolution 53:1979–86
    [Google Scholar]
  52. 52.
    Ishihara M, Shimada M. 1999. Geographical variation in photoperiodic response for diapause induction between univoltine and multivoltine populations of Kytorhinus sharpianus (Coleoptera: Bruchidae). Environ. Entomol. 28:195–200
    [Google Scholar]
  53. 53.
    Ishii M, Hidaka T. 1982. Characteristics of pupal diapause in the univoltine papilionid, Luehdorfia japonica (Lepidoptera: Papilionidae). Kontyû 50:610–20
    [Google Scholar]
  54. 54.
    Ishii M, Hidaka T. 1983. The second pupal diapause in the univoltine papilionid, Luehdorfia japonica (Lepidoptera: Papilionidae) and its terminating factor. Appl. Entomol. Zool. 18:456–63
    [Google Scholar]
  55. 55.
    Ishii M, Johki Y, Hidaka T. 1983. Studies on summer diapause in zygaenid moths (Lepidoptera, Zygaenidae): I. Factors affecting the pupal diapause in Pryeria sinica. Kontyû 51:122–27
    [Google Scholar]
  56. 56.
    Johansson F, Rowe L 1999. Life history and behavioral responses to time constraints in a damselfly. Ecology 80:1242–52
    [Google Scholar]
  57. 57.
    Johansson F, Stoks R, Rowe L, De Block M. 2001. Life history plasticity in a damselfly: effects of combined time and biotic constraints. Ecology 82:1857–69
    [Google Scholar]
  58. 58.
    Jönsson AM, Appelberg G, Harding S, Bärring L. 2009. Spatio-temporal impact of climate change on the activity and voltinism of the spruce bark beetle, Ips typographus. Glob. Change Biol. 15:486–99
    [Google Scholar]
  59. 59.
    Kamitani S, Asakura K, Nakamura K. 2015. Effects of environmental factors on life cycle regulation in Lasius japonicus Santschi (Formicidae). Sociobiology 62:467–73
    [Google Scholar]
  60. 60.
    Karban R 1986. Prolonged development in cicadas. The Evolution of Insect Life Cycles F Taylor, R Karban 222–35 Berlin: Springer
    [Google Scholar]
  61. 61.
    Karban R, Black CA, Weinbaum SA. 2000. How 17-year cicadas keep track of time. Ecol. Lett. 3:253–56
    [Google Scholar]
  62. 62.
    Kato Y, Sakate S. 1981. Studies on summer diapause in pupae of Antheraea yamamai (Lepidoptera: Saturniidae): III. Influence of photoperiod in the larval stage. Appl. Entomol. Zool. 16:499–500
    [Google Scholar]
  63. 63.
    Kato Y, Yamauchi M, Katsu Y, Sakate S. 1979. Studies on summer diapause in pupae of Antheraea yamamai (Lepidoptera: Saturniidae): I. Shortening of the “pupal” duration under certain environmental conditions. Appl. Entomol. Zool. 14:389–96
    [Google Scholar]
  64. 64.
    Khelifa R. 2017. Partial bivoltinism and emergence patterns in the North African endemic damselfly Calopteryx exul: conservation implications. Afr. J. Ecol. 55:145–51
    [Google Scholar]
  65. 65.
    Kimura T, Takano H, Masaki S. 1982. Photoperiodic programming of summer diapause after hibernation in Spilarctia imparilis Butler (Lepidoptera: Arctiidae). Appl. Entomol. Zool. 17:218–26
    [Google Scholar]
  66. 66.
    Kipyatkov VE. 2001. Seasonal life cycles and the forms of dormancy in ants (Hymenoptera: Formicoidea). Acta Soc. Zool. Bohem. 65:211–38
    [Google Scholar]
  67. 67.
    Kohshima S. 1984. A novel cold-tolerant insect found in a Himalayan glacier. Nature 310:225–27
    [Google Scholar]
  68. 68.
    Košt´ál V, Hodek I. 1997. Photoperiodism and control of summer diapause in the Mediterranean tiger moth Cymbalophora pudica. J. Insect Physiol. 43:767–77
    [Google Scholar]
  69. 69.
    Kosumi T, Takeda M. 2017. Three-year lifecycle, large body, and very high threshold temperature in the cricket Gryllus argenteus for special adaptation to desiccation cycle in Malawi. Sci. Nat. 104:70
    [Google Scholar]
  70. 70.
    Kukal O, Duman JG, Serianni AS. 1989. Cold-induced mitochondrial degradation and cryoprotectant synthesis in freeze-tolerant arctic caterpillars. J. Comp. Physiol. B 158:661–71
    [Google Scholar]
  71. 71.
    Lees AD. 1955. The Physiology of Diapause in Arthropods Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  72. 72.
    Leonard DE. 1968. Diapause in the gypsy moth. J. Econ. Entomol. 61:596–98
    [Google Scholar]
  73. 73.
    Ma CS, Ma G, Pincebourde S. 2021. Survive a warming climate: insect responses to extreme high temperatures. Annu. Rev. Entomol. 66:163–84
    [Google Scholar]
  74. 74.
    Maeto K, Ozaki K. 2003. Prolonged diapause of specialist seed-feeders makes predator satiation unstable in masting of Quercus crispula. Oecologia 137:392–98
    [Google Scholar]
  75. 75.
    Maier CT. 1996. Connecticut is awaiting the return of the periodical cicada. Front. Plant Sci. 48:4–6
    [Google Scholar]
  76. 76.
    Mansingh A, Smallman BN. 1966. Photoperiod control of an “obligatory” pupal diapause. Can. Entomol. 98:613–16
    [Google Scholar]
  77. 77.
    Masaki S. 1956. The effect of temperature on the termination of diapause in the egg of Lymantria dispar Linné (Lepidoptera: Lymantriidae). Jpn. J. Appl. Zool. 21:148–57
    [Google Scholar]
  78. 78.
    Masaki S. 1967. Geographic variation and climatic adaptation in a field cricket (Orthoptera: Gryllidae). Evolution 21:725–41
    [Google Scholar]
  79. 79.
    Masaki S. 1980. Summer diapause. Annu. Rev. Entomol. 25:1–25
    [Google Scholar]
  80. 80.
    Matsuda N, Fujita S, Tanaka K, Watari Y, Shintani Y et al. 2019. Robustness of latitudinal life-cycle variations in a cricket Dianemobius nigrofasciatus (Orthoptera: Trigonidiidae) in Japan against climate warming over the last five decades. Appl. Entomol. Zool. 54:349–57
    [Google Scholar]
  81. 81.
    Matsuda N, Tanaka K, Watari Y, Shintani Y, Goto SG et al. 2018. Northward expansion of the bivoltine life cycle of the cricket over the last four decades. Glob. Change Biol. 24:5622–28
    [Google Scholar]
  82. 82.
    Matsuo Y. 2006. Cost of prolonged diapause and its relationship to body size in a seed predator. Funct. Ecol. 20:300–6
    [Google Scholar]
  83. 83.
    Menu F, Debouzie D. 1993. Coin-flipping plasticity and prolonged diapause in insects: example of the chestnut weevil Curculio elephas (Coleoptera: Curculionidae). Oecologia 93:367–73
    [Google Scholar]
  84. 84.
    Menu F, Desouhant E. 2002. Bet-hedging for variability in life cycle duration: Bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause. Oecologia 132:167–74
    [Google Scholar]
  85. 85.
    Menu F, Roebuck J-P, Viala M. 2000. Bet-hedging diapause strategies in stochastic environments. Am. Nat. 155:724–34
    [Google Scholar]
  86. 86.
    Miyazaki Y, Nisimura T, Numata H. 2006. Phase responses in the circannual rhythm of the varied carpet beetle, Anthrenus verbasci, under naturally changing day length. Zool. Sci. 23:1031–37
    [Google Scholar]
  87. 87.
    Miyazaki Y, Nisimura T, Numata H. 2009. Circannual pupation rhythm in the varied carpet beetle Anthrenus verbasci under different nutrient conditions. Entomol. Sci. 12:370–75
    [Google Scholar]
  88. 88.
    Moraiti CA, Nakas CT, Papadopoulos NT. 2012. Prolonged pupal dormancy is associated with significant fitness cost for adults of Rhagoletis cerasi (Diptera: Tephritidae). J. Insect Physiol. 58:1128–35
    [Google Scholar]
  89. 89.
    Moraiti CA, Nakas CT, Papadopoulos NT. 2014. Diapause termination of Rhagoletis cerasi pupae is regulated by local adaptation and phenotypic plasticity: escape in time through bet-hedging strategies. J. Evol. Biol. 27:43–54
    [Google Scholar]
  90. 90.
    Moraiti CA, Papadopoulos NT. 2017. Obligate annual and successive facultative diapause establish a bet-hedging strategy of Rhagoletis cerasi (Diptera: Tephritidae) in seasonally unpredictable environments. Physiol. Entomol. 42:225–31
    [Google Scholar]
  91. 91.
    Moriyama M, Numata H. 2011. A cicada that ensures its fitness during climate warming by synchronizing its hatching time with the rainy season. Zool. Sci. 28:875–81
    [Google Scholar]
  92. 92.
    Musolin DL, Saulich AH. 2000. Summer dormancy ensures univoltinism in the predatory bug Picromerus bidens. Entomol. Exp. Appl. 95:259–67
    [Google Scholar]
  93. 93.
    Nagase A, Masaki S. 1991. Thermal and photoperiodic responses in aestivating pupae of Dictyoploca japonica (Lepidoptera: Saturniidae). Appl. Entomol. Zool. 26:387–96
    [Google Scholar]
  94. 94.
    Nakamura K, Numata H. 1998. Alternative life cycles controlled by temperature and photoperiod in the oligophagous bug, Dybowskyia reticulata. Physiol. Entomol 23:69–74
    [Google Scholar]
  95. 95.
    Nakanishi T, Kaneda T, Nakamuta K. 2017. Effects of temperature on the development and circannual control of pupation in the carpenter moth, Cossus insularis (Lepidoptera: Cossidae), reared on an artificial diet. Appl. Entomol. Zool. 52:29–35
    [Google Scholar]
  96. 96.
    Nisimura T, Numata H. 2001. Endogenous timing mechanism controlling the circannual pupation rhythm of the varied carpet beetle Anthrenus verbasci. J. Comp. Physiol. A 187:433–40
    [Google Scholar]
  97. 97.
    Nisimura T, Numata H. 2003. Circannual control of the life cycle in the varied carpet beetle Anthrenus verbasci. . Funct. Ecol. 17:489–95
    [Google Scholar]
  98. 98.
    Norling U. 1984. The life cycle and larval photoperiodic responses of Coenagrion hastulatum (Charpentier) in two climatically different areas (Zygoptera: Coenagrionidae). Odonatologica 13:429–49
    [Google Scholar]
  99. 99.
    Norling U. 2021. Growth, winter preparations and timing of emergence in temperate zone Odonata: control by a succession of larval response patterns. Int. J. Odonatol. 24:1–36
    [Google Scholar]
  100. 100.
    Numata H, Yamamoto K. 1990. Feeding on seeds induces diapause in the cabbage bug, Eurydema rugosa. Entomol. Exp. Appl. 57:281–84
    [Google Scholar]
  101. 101.
    Nylin S. 1989. Effects of changing photoperiods in the life cycle regulation of the comma butterfly, Polygonia c-album (Nymphalidae). Ecol. Entomol. 14:209–18
    [Google Scholar]
  102. 102.
    Parr MJ. 1970. The life histories of Ischnura elegans (van der Linden) and Coenagrion puella (L.) (Odonata) in south Lancashire. Proc. R. Entomol. Soc. Lond. A 45:172–81
    [Google Scholar]
  103. 103.
    Powell JA. 2001. Longest insect dormancy: Yucca moth larvae (Lepidoptera: Prodoxidae) metamorphose after 20, 25, and 30 years in diapause. Ann. Entomol. Soc. Am. 94:677–80
    [Google Scholar]
  104. 104.
    Salman MHR, Bonsignore CP, El Fels AEA, Giomi F, Hodar JA et al. 2019. Winter temperature predicts prolonged diapause in pine processionary moth species across their geographic range. PeerJ 7:e6530
    [Google Scholar]
  105. 105.
    Salman TS, Vesala L, Hoikkala A. 2012. Photoperiodic regulation of life-history traits before and after eclosion: egg-to-adult development time, juvenile body mass and reproductive diapause in Drosophilamontana. J. Insect Physiol. 58:1541–47
    [Google Scholar]
  106. 106.
    Schebeck M, Dobart N, Ragland GJ, Schopf A, Stauffer C. 2021. Facultative and obligate diapause phenotypes in populations of the European spruce bark beetle Ips typographus. J. Pest Sci. 95:889–99
    [Google Scholar]
  107. 107.
    Schebeck M, Hansen EM, Schopf A, Ragland GJ, Stauffer C, Bentz BJ. 2017. Diapause and overwintering of two spruce bark beetle species. Physiol. Entomol. 42:200–10
    [Google Scholar]
  108. 108.
    Sgolastra F, Kemp WP, Maini S, Bosch J. 2012. Duration of prepupal summer dormancy regulates synchronization of adult diapause with winter temperatures in bees of the genus Osmia. J. Insect Physiol. 58:924–33
    [Google Scholar]
  109. 109.
    Shapiro AM. 1975. Photoperiodic control of development and phenotype in a subarctic population of Pieris occidentalis (Lepidoptera: Pieridae). Can. Entomol. 107:775–79
    [Google Scholar]
  110. 110.
    Shindo J, Masaki S. 1995. Photoperiodic control of larval development in the semivoltine cockroach Periplaneta japonica (Blattidae: Dictyoptera). Ecol. Res. 10:1–12
    [Google Scholar]
  111. 111.
    Shintani Y, Hirose Y, Terao M. 2011. Effects of temperature, photoperiod and soil humidity on induction of pseudopupal diapause in the bean blister beetle Epicauta gorhami. Physiol. Entomol. 36:14–20
    [Google Scholar]
  112. 112.
    Shintani Y, Numata H. 2010. Adaptive significance of the recurrent photoperiodic response in a spring-breeding carabid beetle, Carabus yaconinus. Entomol. Sci. 13:367–74
    [Google Scholar]
  113. 113.
    Shintani Y, Terao M, Tanaka S. 2017. Adaptive significance of precocious pupation in the bean blister beetle, Epicauta gorhami (Coleoptera: Meloidae), a hypermetamorphic insect. J. Insect Physiol. 99:107–12
    [Google Scholar]
  114. 114.
    Simon C, Cooley JR, Karban R, Sota T. 2022. Advances in the evolution and ecology of 13- and 17-year periodical cicadas. Annu. Rev. Entomol. 67:457–82
    [Google Scholar]
  115. 115.
    Sokolova IV. 2007. Univoltine seasonal cycle and obligate diapause in the noctuid moth Charanyca trigrammica Hufn. (Lepidoptera, Noctuidae). Entomol. Rev. 87:793–98
    [Google Scholar]
  116. 116.
    Sota T. 1986. Effects of temperature and photoperiod on larval development and gonad maturation of a carabid beetle, Carabus yaconinus (Coleoptera: Carabidae). Appl. Entomol. Zool. 21:89–94
    [Google Scholar]
  117. 117.
    Sota T. 1987. Effects of temperature and photoperiod on the larval hibernation and adult aestivation of Leptocarabus kumagaii (Coleoptera: Carabidae). Appl. Entomol. Zool. 22:617–23
    [Google Scholar]
  118. 118.
    Sota T. 1987. Mortality pattern and age structure in two carabid populations with different seasonal life cycles. Popul. Ecol. 29:237–54
    [Google Scholar]
  119. 119.
    Soula B, Menu F. 2003. Variability in diapause duration in the chestnut weevil: mixed ESS, genetic polymorphism or bet-hedging?. Oikos 100:574–80
    [Google Scholar]
  120. 120.
    Spacht DE, Gantz JD, Lee RE, Denlinger DL. 2020. Onset of seasonal metabolic depression in the Antarctic midge Belgicaantarctica appears to be independent of environmental cues. Physiol. Entomol. 45:16–21
    [Google Scholar]
  121. 121.
    Stewart KW, Hassage RL, Holder SJ, Oswood MW. 1990. Life cycles of six stonefly species (Plecoptera) in subarctic and arctic Alaska streams. Ann. Entomol. Soc. Am. 83:207–14
    [Google Scholar]
  122. 122.
    Sugiki T, Masaki S. 1972. Photoperiodic control of larval and pupal development in Spilarctia imparilis Butler (Lepidoptera: Arctiidae). Kontyû 40:269–78
    [Google Scholar]
  123. 123.
    Sunose T. 1978. Studies on extended diapause in Hasegawaia sasacola Monzen (Diptera, Cecidomyiidae) and its parasites. Kontyû 46:400–15
    [Google Scholar]
  124. 124.
    Tamura M. 1981. Influence of temperature on the termination of diapause in the egg of Pryeria sinica Moore (Lepidotera: Zygaenidae). Zoen-zasshi 44:220–24 in Japanese )
    [Google Scholar]
  125. 125.
    Tanaka S. 1978. Effects of changing photoperiod on nymphal development in Pteronemobius nitidus Boliver (Orthoptera, Gryllidae). Kontyû 46:135–51
    [Google Scholar]
  126. 126.
    Tanaka S. 1979. Multiple photoperiodic control of the seasonal life cycle in Pteronemobius nitidus Bolivar (Orthoptera: Gryllidae). Kontyû 47:465–75
    [Google Scholar]
  127. 127.
    Tanaka S 1983. Seasonal control of nymphal diapause in the spring ground cricket, Pteronemobius nitidus (Orthoptera: Gryllidae). Diapause and Life Cycle Strategies in Insects VK Brown, I Hodek 35–53 The Hague: Dr. W. Junk Publ.
    [Google Scholar]
  128. 128.
    Tanaka S, Sadoyama Y. 1997. Photoperiodic termination of diapause in field-collected adults of the Bombay locust, Nomadacris succincta (Orthoptera: Acrididae) in southern Japan. Bull. Entomol. Res. 87:533–39
    [Google Scholar]
  129. 129.
    Tanaka S, Zhu DH. 2003. Presence of three diapauses in a subtropical cockroach: control mechanisms and adaptive significance. Physiol. Entomol. 28:323–30
    [Google Scholar]
  130. 130.
    Tanaka SI, Imai C, Numata H. 2002. Ecological significance of adult summer diapause after nymphal winter diapause in Poecilocoris lewisi (Distant) (Heteroptera: Scutelleridae). Appl. Entomol. Zool. 37:469–75
    [Google Scholar]
  131. 131.
    Tauber MJ, Tauber CA. 1976. Developmental requirements of the univoltine species Chrysopa downesi: photoperiodic stimuli and sensitive stages. J. Insect Physiol. 22:331–35
    [Google Scholar]
  132. 132.
    Tauber MJ, Tauber CA. 1976. Insect seasonality: diapause maintenance, termination, and postdiapause development. Annu. Rev. Entomol. 21:81–107
    [Google Scholar]
  133. 133.
    Tauber MJ, Tauber CA, Masaki S. 1986. Seasonal Adaptations of Insects Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  134. 134.
    Tedders WL. 1978. Important biological and morphological characteristics of the foliar-feeding aphids of pecan Tech. Bull. 1579, US Dep. Agric. Washington, DC:
    [Google Scholar]
  135. 135.
    Terao M, Hirose Y, Shintani Y. 2015. Food-availability dependent premature metamorphosis in the bean blister beetle Epicauta gorhami (Coleoptera: Meloidae), a hypermetamorphic insect that feeds on grasshopper eggs in the larval stage. Entomol. Sci. 18:85–93
    [Google Scholar]
  136. 136.
    Teslenko VA. 2014. The life cycle and production of three common stonefly species (Insecta, Plecoptera) in the Kedrovaya River (the south of Primorskii Territory). Entomol. Rev. 94:1191–201
    [Google Scholar]
  137. 137.
    Togashi K. 2014. Effects of larval food shortage on diapause induction and adult traits in Taiwanese Monochamus alternatus alternatus. Entomol. Exp. Appl. 151:34–42
    [Google Scholar]
  138. 138.
    Togashi K. 2017. Effects of crowding on larval diapause and adult body size in Monochamus alternatus alternatus (Coleoptera: Cerambycidae). Can. Entomol. 149:159–73
    [Google Scholar]
  139. 139.
    Tokuda M, Yukawa J, Gôukon K. 2007. Life history traits of Pseudasphondylia rokuharensis (Diptera: Cecidomyiidae) affecting emergence of adults and synchronization with host plant phenology. Environ. Entomol. 36:518–23
    [Google Scholar]
  140. 140.
    Topp W. 1986. Imaginal aestivation in the rove beetle species Omalium rivulare (Coleoptera: Staphylinidae). Entomol. Gen. 12:51–55
    [Google Scholar]
  141. 141.
    Topp W. 1990. Selection for an optimal monovoltine life cycle in an unpredictable environment. Studies on the beetle Catops nigricans Spence (Col., Catopidae). Oecologia 84:134–41
    [Google Scholar]
  142. 142.
    Trudel R, Lavallee R, Bauce ER, Guertin C. 2002. The effect of cold temperature exposure and long-day photoperiod on the termination of the reproductive diapause of newly emerged female Pissodes strobi (Coleoptera: Curculionidae). Agric. For. Entomol. 4:301–8
    [Google Scholar]
  143. 143.
    Tzanakakis ME, Karakassis EJ, Tsaklidis G, Karabina ECh, Argalavini ICh, Arabatzis IG 1991. Diapause termination in the almond seed wasp, Eurytoma amygdali Enderlein (Hym., Eurytomidae), in northern Greece and under certain photoperiods and temperatures. J. Appl. Entomol. 111:86–98
    [Google Scholar]
  144. 144.
    Tzanakakis ME, Veerman A. 1994. Effect of temperature on the termination of diapause in the univoltine almond seed wasp Eurytoma amygdali. Entomol. Exp. Appl. 70:27–39
    [Google Scholar]
  145. 145.
    Umeya Y. 1946. Embryonic hibernation and diapause in insects from the viewpoint of the hibernating-eggs of the silkworm. Bull. Seric. Exp. Stat. 12:393–480 in Japanese )
    [Google Scholar]
  146. 146.
    Visser ME, Holleman LJ. 2001. Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc. R. Soc. B 268:289–94
    [Google Scholar]
  147. 147.
    Wiklund C, Lehmann P, Friberg M. 2019. Diapause decision in the small tortoiseshell butterfly, Aglais urticae. Entomol. Exp. Appl. 167:433–41
    [Google Scholar]
  148. 148.
    Williams CM. 1946. Physiology of insect diapause: the role of the brain in the production and termination of pupal dormancy in the giant silkworm, Platysamia cecropia. Biol. Bull. 90:234–43
    [Google Scholar]
  149. 149.
    Williams KS, Simon C. 1995. The ecology, behavior, and evolution of periodical cicadas. Annu. Rev. Entomol. 45:269–95
    [Google Scholar]
  150. 150.
    Wipking W. 1988. Repeated larval diapause and diapause-free development in geographic strains of the burnet moth Zygaena trifolii Esp. (Insecta, Lepidoptera). Oecologia 77:557–64
    [Google Scholar]
  151. 151.
    Wipking W, Mengelkoch C. 1994. Control of alternate-year flight activities in high-alpine Ringlet butterflies (Erebia, Satyridae) and Burnet moths (Zygaena, Zygaenidae) from temperate environments. Insect Life-Cycle Polymorphism: Theory, Evolution and Ecological Consequences for Seasonality and Diapause Control HV Danks 313–47 Dordrecht, Neth: Kluwer Acad. Publ.
    [Google Scholar]
  152. 152.
    Yamamoto S, Sota T. 2009. Incipient allochronic speciation by climatic disruption of the reproductive period. Proc. R. Soc. B 276:2711–19
    [Google Scholar]
  153. 153.
    Yamamura S, Ikarashi M, Sasaki M. 2008. Dual photoperiodic regulation to enable univoltine life cycle in alpine silver-Y moth, Syngrapha ottolenguii (Noctuidae: Plusiinae) without obligatory diapause. Appl. Entomol. Zool. 43:105–12
    [Google Scholar]
  154. 154.
    Yamashita O, Yaginuma T 1991. Silkworm eggs at low temperatures: implication for sericulture. Insects at Low Temperatures RE Lee, DL Denlinger 424–45 New York: Chapman & Hall
    [Google Scholar]
  155. 155.
    Yukawa J, Nakagawa K, Saigou T, Awa T, Fukuda T, Higashi M. 2013. Adult behavior of an ambrosia gall midge Illiciomyia yukawai (Diptera: Cecidomyiidae) and synchronization between its emergence and host plant phenology. Entomol. Sci. 16:400–12
    [Google Scholar]
  156. 156.
    Yukawa J, Uechi N 2021. Life history traits. Biology of Gall Midges: Evolution, Ecology, and Biological Control J Yukawa, M Tokuda 119–49 Berlin: Springer
    [Google Scholar]
  157. 157.
    Zhu DH, Tanaka S. 2004. Summer diapause and nymphal growth in a subtropical cockroach: response to changing photoperiod. Physiol. Entomol. 29:78–83
    [Google Scholar]
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