Skip to main content
Log in

Seasonal cycles in stink bugs (Heteroptera, Pentatomidae) from the temperate zone: Diversity and control

  • Published:
Entomological Review Aims and scope Submit manuscript

Abstract

The paper reviews the diversity of seasonal cycles known in stink bugs (Heteroptera, Pentatomidae) from the temperate zone and is based on the data of 43 pentatomid species studied in detail up to date (Saulich and Musolin, 2011). All the seasonal cycles realized by pentatomids in the temperate zone can be divided into two large groups: univoltine and multivoltine cycles. In univoltine cycles, only one generation is annually realized. However, univoltinism of a particular species or population can be ensured by different mechanisms: its control can be endogenous (involving an obligate diapause) or exogenous (environmental, involving a facultative diapause). Furthermore, endogenously controlled univoltine seasonal cycles can include obligate embryonic (egg) diapause (e.g., Picromerus bidens and Apateticus cynicus), obligate nymphal diapause (e.g., Pentatoma rufipes) or obligate adult (reproductive) diapause (e.g., Palomena prasina, Palomena angulosa, and Menida scotti). Exogenously controlled seasonal cycles are more flexible. Many species that are multivoltine in the subtropical or warm temperate zones are univoltine further polewards. In this case, their univoltinism is controlled exogenously, or environmentally. The mechanism often involves such seasonal adaptations as photoperiodic response of facultative winter diapause induction with a high thermal optimum (e.g., Arma custos and Dybowskyia reticulata) or a high critical threshold of winter diapause induction response (e.g., Graphosoma lineatum). The seasonal cycles of some species include not only winter diapause (hibernation) but also summer diapause (aestivation). The diapausing stage can be the same (e.g., Nezara antennata has facultative adult winter and summer diapauses) or different (e.g., Picromerus bidens survives winter in obligate embryonic diapause and spends the hottest period of summer in facultative adult aestivation). All the multivoltine cycles follow the same general pattern, with one, two, or even more directly breeding generation(s) followed by a generation that enters winter diapause. However, this sequence may be complicated by incorporation of specific seasonal adaptations such as aestivation, migrations, different forms of seasonal polyphenism or polymorphism (e.g., seasonal changes of body color), etc. Many stink bugs demonstrate geographic clines of voltinism, producing several generations in the subtropical regions (environmentally controlled multivoltine development) and two or only one generation(s) polewards (environmentally controlled bi- or univoltinism). However, some species demonstrate a strictly bivoltine seasonal cycle: they always produce two annual generations, each with either winter or summer diapause. An example is Nezara antennata which produces two generations and enters facultative winter and summer diapauses. Semivoltine seasonal cycles last more than one year. They are not very rare among insects and are known in true bugs, but have not yet been recorded among pentatomids. Examples of different seasonal cycles are described and discussed in detail. Further discussion is focused on the ecological importance of photoperiodic and thermal responses in cases of natural or artificial dispersal of pentatomids beyond their original ranges. The phytophagous Nezara viridula and the predatory Podisus maculiventris and Perillus bioculatus are used as examples. An attempt is made to compare the phylogeny of Pentatomidae and distribution of realized patterns of their seasonal development. However, it is concluded that reconstruction of phylogenetic relationships cannot yet provide a sufficient basis for prediction of realized seasonal cycles. It is suggested that the terms uni-, bi-, multi-, and semivoltinism should refer to populations rather than species, since the realized patterns of seasonal development often differ between the northern and southern populations of the same broadly distributed species.

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.

Institutional subscriptions

Similar content being viewed by others

References

  1. Alekseev, V.R., Diapause of Crustaceans: the Eco-Physiological Aspects (Nauka, Moscow, 1990) [in Russian].

    Google Scholar 

  2. Arnoldi, K.V., “The Sunn Pest (Eurygaster integriceps) in the Central Asian Wildlife as Related to the Ecological and Biocenological Aspects of Its Biology,” in The Sunn Pest Eurygaster integriceps Put. Vol. 1, Ed. by D.M. Fedotov (USSR Acad. Sci., Moscow, 1947), pp. 136–269 [in Russian].

    Google Scholar 

  3. Asanova, R.B. and Iskakov, B.V., Harmful and Beneficial Bugs of Kazakhstan (Kainar, Alma-Ata, 1977) [in Russian].

    Google Scholar 

  4. Babaroğlu, N. and Uğur, F., “Investigation on Fecundity of Cereal Bug [Aelia rostrata Boh. (Het.: Pentatomidae)] on Some Wheat and Barley Varieties,” Plant Prot. Bull. 41(1–2), 1–16 (2001) [in Turkish with English summary].

    Google Scholar 

  5. Babrakzai, Z. and Hodek, I., “Diapause Induction and Termination in a Population of Dolycoris baccarum (Heteroptera, Pentatomidae) from Central Bohemia,” Věst. Čs. Spol. Zool. 51, 85–88 (1987).

    Google Scholar 

  6. Belozerov, V.N., “The Distribution of Dormant Stages in the Development Cycles of Acarines (Chelicerata: Arachnida: Acari) as Compared with Mandibulate Arthropods: Insecta and Crustacea,” in Strategies of Adaptations of Terrestrial Arthropods to Adverse Environmental Conditions, Ed. by A.A. Stekolnikov (St. Petersburg State University, St. Petersburg, 2007), pp. 193–233 [in Russian].

    Google Scholar 

  7. Belozerov, V.N., “Dormant Stages and Their Participation in Adjustment and Regulation of Life Cycles of Harvestmen (Arachnida, Opiliones),” Entomol. Obozr. 91(1), 180–216 (2012) [Entomol. Rev. 92 (6), 688–714 (2012)].

    Google Scholar 

  8. Brown, E.S., “Researches on the Ecology and Biology of Eurygaster integriceps Put. (Hemiptera, Scutelleridae) in Middle East Countries, with Special Reference to the Overwintering Period,” Bull. Entomol. Res. 53, 445–514 (1962).

    Google Scholar 

  9. Burov, V.N., “Factors Affecting Population Dynamics and Harmfulness of Wheat Stink Bugs of the Genus Aelia (Heteroptera, Pentatomidae),” Entomol. Obozr. 41(2), 262–273 (1962).

    Google Scholar 

  10. Butler, E.A., Biology of British Hemiptera-Heteroptera (H.F. and G. Witherby, London, 1923).

    Google Scholar 

  11. Cakmak, O., Bashan, M., and Kocak, E., “The Influence of Life-Cycle on Phospholipid and Triacylglycerol Fatty Acid Profiles of Aelia rostrata Boheman (Heteroptera: Pentatomidae),” J. Kans. Entomol. Soc. 81(3), 261–275 (2008).

    Google Scholar 

  12. Chelnokova, T.A., “An Ecological Characteristic and Biotopic Distribution of Predatory Bugs of the Family Pentatomidae (Hemiptera-Heteroptera) in the Forest Zone of the Middle Volga Basin,” Trudy Kuibyshev. Ped. Inst. 243, 82–86 (1980).

    Google Scholar 

  13. Coetzee, J.A., Byrne, M.J., and Hill, M.P., “Predicting the Distribution of Eccritotarsus catarinensis, a Natural Enemy Released on Water Hyacinth in South Africa,” Entomol. Exp. Appl. 125(3), 237–247 (2007).

    Google Scholar 

  14. Conradi-Larsen, E.M. and Sømme, L., “Notes on the Biology of Dolycoris baccarum L. (Het., Pentatomidae),” Nor. Entomol. Tidssk. 20, 245–247 (1973).

    Google Scholar 

  15. Danilevsky, A.S., Photoperiodism and Seasonal Development of Insects (Len. Gos. Univ., Leningrad, 1961) [in Russian].

    Google Scholar 

  16. Danilevsky, A.S. and Kuznetsova, I.A., “Intraspecific Adaptations of Insects to Climatic Zonality,” in Photoperiodic Adaptations in Insects and Acarines, Ed. by A.S. Danilevsky (Len. Gos. Univ., Leningrad, 1968), pp. 5–51 [in Russian].

    Google Scholar 

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

    Google Scholar 

  18. Danks, H.V., Insect Dormancy: An Ecological Perspective (Biological Survey of Canada, Ottawa, 1987).

    Google Scholar 

  19. Denlinger, D.L., “Dormancy in Tropical Insects,” Annu. Rev. Entomol. 31, 239–264 (1986).

    PubMed  CAS  Google Scholar 

  20. De Clercq, P. and Degheele, D., “Cold Storage of the Predatory Bugs Podisus maculiventris (Say) and Podisus sagitta (Fabricius) (Heteroptera: Pentatomidae),” Parasitica 1–2, 27–41 (1993).

    Google Scholar 

  21. Ferrari, A., Schwertner, C.F., and Grazia, J., “Review, Cladistic Analysis and Biogeography of Nezara Amyot & Serville (Hemiptera: Pentatomidae),” Zootaxa, No. 2424, 1–41 (2010).

    Google Scholar 

  22. Gapon, D.A., Candidate’s Dissertation in Biology (St. Petersburg, 2008).

    Google Scholar 

  23. Geshi, Y. and Fujisaki, K., “Northward Range Expansion of Nezara viridula in Kinki District, Japan: Expansion Speed,” Jpn. J. Appl. Entomol. Zool. 57(3), 151–157 (2013).

    Google Scholar 

  24. Gomi, T., “Geographic Variation in Critical Photoperiod for Diapause Induction and Its Temperature Dependence in Hyphantria cunea Drury (Lepidoptera: Arctiidae),” Oecologia (Berlin) 111, 160–165 (1997).

    Google Scholar 

  25. Harris, V.E., Todd, J.W., and Mullinix, B.G., “Color Change as an Indicator of Adult Diapause in the Southern Green Stink Bug, Nezara viridula,” J. Agric. Entomol. 1(1), 82–91 (1984).

    Google Scholar 

  26. Hawkins, R.D., Shieldbugs of Surrey (Surrey Wildlife Trust, Surrey, 2003).

    Google Scholar 

  27. Henry, T.J., “Biodiversity of Heteroptera,” in Insect Biodiversity: Science and Society, Ed. by R.G. Foottit and P.H. Adler (Blackwell Publ., Oxford, 2009), pp. 223–263.

    Google Scholar 

  28. Higuchi, H., “Photoperiodic Induction of Diapause, Hibernation and Voltinism in Piezodorus hybneri (Heteroptera: Pentatomidae),” Entomol. Sci. 29(4), 585–592 (1994).

    Google Scholar 

  29. Hodek, I., “Sensitivity to Photoperiod in Aelia acuminata (L.) after Adult Diapause,” Oecologia (Berlin) 6, 152–155 (1971).

    Google Scholar 

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

    Google Scholar 

  31. Hodek, I. and Hodková, M., “Role of Temperature and Photoperiod in Diapause Regulation in Czech Populations of Dolycoris baccarum (Heteroptera, Pentatomidae),” Eur. J. Entomol. 90, 95–98 (1993).

    Google Scholar 

  32. Hodek, I. and Honěk, A., “Incidence of Diapause in Aelia acuminata (L.) Population from Southwest Slovakia (Heteroptera),” Věst. Čs. Spol. Zool. 34, 170–183 (1970).

    Google Scholar 

  33. Hodková, M., Hodek, I., and Sømme, L., “Cold is Not a Prerequisite for the Completion of Photoperiodically Induced Diapause in Dolycoris baccarum from Norway,” Entomol. Exp. Appl. 52, 185–188 (1989).

    Google Scholar 

  34. Hokkanen, H., “Polymorphism, Parasites, and the Native Area of Nezara viridula (Hemiptera, Pentatomidae),” Ann. Entomol. Fenn. 52, 28–31 (1986).

    Google Scholar 

  35. Honěk, A., “Induction of Diapause in Aelia acuminata (L.) (Heteroptera, Pentatomidae),” Acta Entomol. Bohemoslov. 66, 345–351 (1969).

    Google Scholar 

  36. Hori, K., “Effect of Photoperiod on Nymphal Growth of Palomena angulosa Motschulsky (Hemiptera: Pentatomidae),” Appl. Entomol. Zool. 21(4), 597–605 (1986).

    Google Scholar 

  37. Hori, K., Kuramochi, K., and Nakabayashi, S., “Effect of Several Different Food Plants on Nymphal Development of Palomena angulosa Motschulsky (Hemiptera: Pentatomidae),” Res. Bull. Obihiro Univ. 14, 239–246 (1985).

    Google Scholar 

  38. Iosifov, M.V., Fauna of Bulgaria, Vol. 12: Heteroptera, Pentatomidae (Sofia, 1981) [in Bulgarian].

    Google Scholar 

  39. Ismailov, V.Ya. and Agasieva, I.S., “The Predaceous Bug Perillus bioculatus F.: A New View of the Prospects of Acclimation and Use,” Zashchita i Karantin Rast., No. 2, 30–31 (2010).

    Google Scholar 

  40. Ismailov, V.Ya. and Oleshchenko, I.N., “Laboratory Breeding of the Predaceous Bug Arma custos F. (Hemiptera: Pentatomidae) and Some Aspects of Its Biology,” Nauchnye Dokl. Vysshei Shkoly Biol. Nauki 4, 54–58 (1977).

    Google Scholar 

  41. Jasič, I., “On the Life Cycle of Perillus bioculatus,” Acta Entomol. Bohemoslov. 72(6), 383–390 (1975).

    Google Scholar 

  42. Javahery, M., “Biology and Ecology of Picromerus bidens (Hemiptera: Pentatomidae) in Southeastern Canada,” Entomol. News 97, 87–98 (1986).

    Google Scholar 

  43. Javahery, M., “Biology and Ecological Adaptation of the Green Stink Bug (Hemiptera: Pentatomidae) in Quebec and Ontario,” Ann. Entomol. Soc. Amer. 83(2), 201–206 (1990).

    Google Scholar 

  44. Javahery, M., “Development of Eggs in Some True Bugs (Hemiptera-Heteroptera). Part I. Pentatomidae,” Can. Entomol. 126, 401–433 (1994).

    Google Scholar 

  45. Jones, P.A. and Coppel, H.C., “Immature Stages of Apateticus cynicus (Say) (Hemiptera: Pentatomidae),” Can. Entomol. 95, 770–779 (1963).

    Google Scholar 

  46. Kamenkova, K.V., “Biology and Ecology of the Stink Bug Dolycoris baccarum L., an Accessory Host of the Sunn Pest Oviphages in Krasnodar Territory,” Entomol. Obozr. 37(3), 654–579 (1958).

    Google Scholar 

  47. Kariya, H., “Effect of Temperature on the Development and the Mortality of the Southern Green Stink Bug, Nezara viridula and the Oriental Green Stink Bug, N. antennata,” Jpn. J. Appl. Entomol. Zool. 5, 191–196 (1961).

    Google Scholar 

  48. Karsavuran, Y., “Investigations on the Biology and Ecology of Dolycoris baccarum (L.) (Het. Pentatomidae) which Attacks Various Plants of Economic Importance at Bornova (Izmir),” Türkiye Bitki Koruma Dergisi 10(4), 213–230 (1986).

    Google Scholar 

  49. Kavar, T., Pavlovčič, P., Sušnik, S., et al., “Genetic Differentiation of Geographically Separated Populations of the Southern Green Stink Bug Nezara viridula (Hemiptera: Pentatomidae),” Bull. Entomol. Res. 96(2), 117–128 (2006).

    PubMed  CAS  Google Scholar 

  50. 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, Ed. by A.A. Stekolnikov (St. Petersburg State University, St. Petersburg, 2007), pp. 107–192 [in Russian].

    Google Scholar 

  51. Kiritani, K., “Distribution and Abundance of the Southern Green Stink Bug, Nezara viridula,” in Proc. Symp. on Rice Insects (Tropical Agricultural Research Center, Tokyo, 1971), pp. 235–248.

    Google Scholar 

  52. Kiritani, K., Hokyo, N., and Kimura, K., “Differential Winter Mortality Relative to Sex in the Population of the Southern Green Stink Bug, Nezara viridula (Pentatomidae, Hemiptera),” Jpn. J. Appl. Entomol. Zool. 6(3), 242–246 (1962).

    Google Scholar 

  53. Kiritani, K., Hokyo, N., and Yukawa, J., “Co-Existence of the Two Related Stink Bugs Nezara viridula and N. antennata under Natural Conditions,” Res. Pop. Ecol. 5, 11–22 (1963).

    Google Scholar 

  54. Kiritani, Y., “Timing of Oviposition and Nymphal Diapause under the Natural Daylengths in Carbula humerigera (Heteroptera: Pentatomidae),” Appl. Entomol. Zool. 20, 252–256 (1985a).

    Google Scholar 

  55. Kiritani, Y., “Effect of Stationary and Changing Photoperiods on Nymphal Development in Carbula humerigera (Heteroptera: Pentatomidae),” Appl. Entomol. Zool. 20, 257–263 (1985b).

    Google Scholar 

  56. Klyuchko, Z.F., Noctuid Moths of Ukraine (Izdat. Vaevskogo, Kiev, 2006) [in Ukrainian].

    Google Scholar 

  57. Klyuchko, Z.F., Budashkin, Yu.I., and Gerasimov, V.P., “New and Little Known Species of Noctuidae (Lepidoptera) of Ukraine,” Vestnik Zool. 38(1), 94 (2004).

    Google Scholar 

  58. Kobayashi, S. and Numata, H., “Photoperiodic Responses Controlling the Induction of Adult Diapause and the Determination of Seasonal Form in the Bean Bug, Riptortus clavatus,” Zool. Sci. 10, 983–990 (1993).

    Google Scholar 

  59. Kobayashi, T., “Biology of Insect Pests of Soybean and Their Control,” Jpn. Agric. Res. Quart. 6, 212–218 (1972).

    Google Scholar 

  60. Kon, M., Oe, A., and Numata, H., “Ethological Isolation between Two Congeneric Green Stink Bugs, Nezara antennata and N. viridula (Heteroptera: Pentatomidae),” J. Ethol. 12, 67–71 (1994).

    Google Scholar 

  61. Koshiyama, Y., Fujisaki, K., and Nakasuji, F., “Mating and Diapause in Hibernating Adults of Menida scotti Puton (Heteroptera: Pentatomidae),” Res. Pop. Ecol. Kyoto 36, 87–92 (1994).

    Google Scholar 

  62. Koshiyama, Y., Tsumuki, H., Muraji, M., et al., “Transfer of Male Secretions to Females through Copulation in Menida scotti (Heteroptera: Pentatomidae),” Appl. Entomol. Zool. 28, 325–332 (1993).

    Google Scholar 

  63. Krambias, A., “Host Plant, Seasonal Migration and Control of the Berry Bug Dolycoris baccarum L. in Cyprus,” Plant Prot. Bull. 35(1), 25–26 (1987).

    Google Scholar 

  64. Larivière, M.-C. and Larochelle, A., “Picromerus bidens (Heteroptera: Pentatomidae) in North America, with a World Review of Distribution and Bionomics,” Entomol. News 100(4), 133–146 (1989).

    Google Scholar 

  65. Leston, D., “The Life-Cycle of Picromerus bidens (L.) (Hem., Pentatomidae) in Britain,” Entomol. Month. Mag. 91, 109 (1955).

    Google Scholar 

  66. Masaki, S., “Summer Diapause,” Annu. Rev. Entomol. 25, 1–25 (1980).

    Google Scholar 

  67. Masaki, S. and Sakai, T., “Summer Diapause in the Seasonal Life Cycle of Mamestra brassicae L. (Lepidoptera: Noctuidae),” Jap. J. Appl. Entom. Zool. 9(3), 191–205 (1965).

    Google Scholar 

  68. Masaki, S. and Yata, O., “Seasonal Adaptation and Photoperiodism in Butterflies,” Spec. Bull. Lepidopt. Soc. Jap. 6, 341–383 (1988) [in Japanese, with English summary].

    Google Scholar 

  69. Masaki, S. and Walter, T.J., “Cricket Life Cycles,” Evol. Biol. 21, 349–423 (1987).

    Google Scholar 

  70. 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 

  71. McPherson, J.E., Pentatomoidea (Hemiptera) of Northeastern North America. Carbondale and Edwardsville (South Illinois Univ. Press, Illinois, 1982).

    Google Scholar 

  72. Miner, F.D., “Biology and Control of Stink Bugs on Soybeans,” Arkansas Agric. Exp. Stat. Bull., No. 708, 1–40 (1966).

    Google Scholar 

  73. Musolin, D.L., “Insects in a Warmer World: Ecological, Physiological and Life-History Responses of True Bugs (Heteroptera) to Climate Change,” Global Change Biol. 13(8), 1565–1585 (2007).

    Google Scholar 

  74. Musolin, D.L., “Surviving Winter: Diapause Syndrome in the Southern Green Stink Bug Nezara viridula in the Laboratory, in the Field, and under Climate Change Conditions,” Physiol. Entomol. 37(4), 309–322 (2012).

    Google Scholar 

  75. Musolin, D.L., Fujisaki, K., and Numata, H., “Photoperiodic Control of Diapause Termination, Color Change and Postdiapause Reproduction in the Southern Green Stink Bug, Nezara viridula,” Physiol. Entomol. 32, 64–72 (2007).

    Google Scholar 

  76. Musolin, D.L. and Numata, H., “Photoperiodic and Temperature Control of Diapause Induction and Color Change in the Southern Green Stink Bug Nezara viridula,” Physiol. Entomol. 28(2), 65–74 (2003a).

    Google Scholar 

  77. Musolin, D.L. and Numata, H., “Timing of Diapause Induction and Its Life-History Consequences in Nezara viridula: Is It Costly to Expand the Distribution Range?” Ecol. Entomol. 28(6), 694–703 (2003b).

    Google Scholar 

  78. Musolin, D.L. and Numata, H., “Late-Season Induction of Diapause in Nezara viridula and Its Effect on Adult Coloration and Post-Diapause Reproductive Performance,” Entomol. Exp. Appl. 111, 1–6 (2004).

    Google Scholar 

  79. Musolin, D.L. and Saulich, A.Kh., “Factors Regulating the Seasonal Cycle in the Striped Shield Bug Graphosoma lineatum L. (Heteroptera, Pentatomidae). 1. The Thermal Norms of Development and Photoperiodic Reaction,” Entomol. Obozr. 74(4), 736–743 (1995).

    Google Scholar 

  80. Musolin, D.L. and Saulich, A.Kh., “Photoperiodic Control of Nymphal Growth in True Bugs (Heteroptera),” Zool. Zh. 76(5), 530–540 (1997) [Entomol. Rev. 77 (6), 768–780 (1997)].

    Google Scholar 

  81. Musolin, D.L. and Saulich, A.H., “Summer Dormancy Ensures Univoltinism in the Predatory Bug Picromerus bidens (Heteroptera, Pentatomidae),” Entomol. Exp. Appl. 95, 259–267 (2000).

    Google Scholar 

  82. Musolin, D.L. and Saulich, A.H., “Environmental Control of Voltinism of the Stinkbug Graphosoma lineatum in the Forest-Steppe Zone (Heteroptera: Pentatomidae),” Entomol. Gen. 25(4), 255–264 (2001).

    Google Scholar 

  83. Musolin, D.L. and Saulich, A.Kh., “Changes in the Natural Ranges of Insects under the Conditions of Recent Climate Warming,” in Proceedings of St. Petersburg Forest Technical Academy, Issue 196 (St. Petersburg, 2011), pp. 246–254 [in Russian].

    Google Scholar 

  84. Musolin, D.L. and Saulich, A.Kh., “Insect Voltinism under the Conditions of Recent Climate Changes,” in Proceedings of St. Petersburg Forest Technical Academy, Issue 200 (St. Petersburg, 2012a), pp. 208–221 [in Russian].

    Google Scholar 

  85. Musolin, D.L. and Saulich, A.Kh., “Responses of Insects to the Current Climate Changes: from Physiology and Behavior to Range Shifts,” Entomol. Obozr. 91(1), 3–35 (2012b) [Entomol. Rev. 92 (7), 715–740 (2012)].

    Google Scholar 

  86. Musolin, D.L., Tougou, D., and Fujisaki, K., “Too Hot to Handle? Phenological and Life-History Responses to Simulated Climate Change of the Southern Green Stink Bug Nezara viridula (Heteroptera: Pentatomidae),” Global Change Biol. 16(1), 73–87 (2010).

    Google Scholar 

  87. 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, 91–98 (2004).

    Google Scholar 

  88. Nakamura, K. and Numata, H., “Photoperiodic Sensitivity in Adults of Aelia fieberi (Heteroptera: Pentatomidae),” Eur. J. Entomol. 92, 609–613 (1995).

    Google Scholar 

  89. Nakamura, K. and Numata, H., “Seasonal Life Cycle of Aelia fieberi (Heteroptera: Pentatomidae),” Ann. Entomol. Soc. Amer. 90, 625–630 (1997).

    Google Scholar 

  90. Nakamura, K. and Numata, H., “Alternative Life Cycles Controlled by Temperature and Photoperiod in the Oligophagous Bug, Dybowskyia reticulata,” Physiol. Entomol. 23, 69–74 (1998).

    Google Scholar 

  91. Nakamura, K. and Numata, H., “Environmental Regulation of Adult Diapause of Graphosoma rubrolineatum (Westwood) (Heteroptera: Pentatomidae) in Southern and Northern Populations of Japan,” Appl. Entomol. Zool. 34(3), 323–326 (1999).

    Google Scholar 

  92. Nakamura, K. and Numata, H., “Effect of Photoperiod and Temperature on the Induction of Adult Diapause in Dolycoris baccarum (L.) (Heteroptera: Pentatomidae) from Osaka and Hokkaido, Japan,” Appl. Entomol. Zool. 41(1), 105–109 (2006).

    Google Scholar 

  93. Nayanov, N.I., “On Acclimation of the Ragweed Moth Tarachidia candefacta Hübn. (Lepidoptera, Noctuidae) in the South of European Russia,” Entomol. Obozr. 70(4), 759–767 (1973).

    Google Scholar 

  94. Niva, C.C., Molecular and Neuroendocrine Mechanisms of Photoperiodism in Halyomorpha halys (Heteroptera: Pentatomidae). PhD Dissertation (Kobe University, Kobe, 2003).

    Google Scholar 

  95. Noda, H. and Ishii, T., “Effects of Photoperiod and Temperature on the Ovarian Development of the White-Spotted Stink Bug, Eysarcoris ventralis (Heteroptera: Pentatomidae),” Jpn. J. Appl. Entomol. Zool. 25, 33–38 (1981) [in Japanese, with English summary].

    Google Scholar 

  96. Noda, T., “Short Day Photoperiod Accelerates the Oviposition in the Oriental Green Stink Bug, Nezara antennata Scott (Heteroptera: Pentatomidae),” Appl. Entomol. Zool. 19(1), 119–120 (1984).

    Google Scholar 

  97. Numata, H. and Kobayashi, S., “Threshold and Quantitative Photoperiodic Responses Exist in an Insect,” Experientia 50, 969–971 (1994).

    CAS  Google Scholar 

  98. Numata, H. and Nakamura, K., “Photoperiodism and Seasonal Adaptations in Some Seed-Sucking Bugs (Heteroptera) in Central Japan,” Europ. J. Entomol. 99, 155–161 (2002).

    Google Scholar 

  99. Panizzi, A.R. and Hirose, E., “Seasonal Body Weight, Lipid Content, and Impact of Starvation and Water Stress on Adult Survivorship and Longevity of Nezara viridula and Euschistus heros,” Entomol. Exp. Appl. 76, 247–253 (1995).

    CAS  Google Scholar 

  100. Panizzi, A.R., McPherson, J.E., James, D.G., et al., “Stink Bugs (Pentatomidae),” in Heteroptera of Economic Importance, Ed. by C.W. Schaefer and A.R. Panizzi (CRC Press, Boca Raton, 2000), pp. 421–474.

    Google Scholar 

  101. Perepelitsa, L.V., “The Role of Photoperiod in the Development of Dolycoris baccarum,” Byul. Vses. NII Zashch. Rast. 21, 11–13 (1971).

    Google Scholar 

  102. Petrova, V.P., Candidate’s Dissertation in Biology (Novosibirsk, 1969).

    Google Scholar 

  103. Poltavsky, A.N. and Artokhin, K.S., “Tarachidia candefacta (Lepidoptera: Noctuidae) in the South of European Russia,” Phegea 34(2), 41 (2006).

    Google Scholar 

  104. Puchkov, P.V., Fauna of Ukraine, Vol. 21, Issue 1: Shield Bugs (Ukrainian SSR Acad. Sci., Kiev, 1961) [in Russian].

    Google Scholar 

  105. Puchkov, P.V., Shield Bugs of Central Asia (Ilim, Frunze, 1965) [in Russian].

    Google Scholar 

  106. Richman, D.V. and Mead, F.W., “Stages in the Life Cycle of a Predatory Stink Bug, Podisus maculiventris (Say) (Hemiptera: Pentatomidae),” in Entomology Circular No. 216 (Florida Dept. Agric. Consumer Services, Div. of Plant Industry, 1980), pp. 1–2.

    Google Scholar 

  107. Rider, D.A., “Family Pentatomidae Leach, 1815,” in Catalogue of the Heteroptera of the Palaearctic Region, Vol. 5: Pentatomomorpha II, Ed. by B. Aukema and C. Rieger (The Netherlands Entomol. Soc., Wageningen, 2006), pp. 233–414.

    Google Scholar 

  108. Saulich, A.Kh., “The Significance of Abiotic Factors for Shaping of Secondary Ranges in Adventive Insect Species,” Entomol. Obozr. 73(3), 591–605 (1994).

    Google Scholar 

  109. Saulich, A.Kh., Seasonal Development and Dispersal Potential of Insects (St. Petersburg State Univ., St. Petersburg, 1999) [in Russian].

    Google Scholar 

  110. Saulich, A.Kh., “Long Life Cycles in Insects,” Entomol. Obozr. 89(3), 497–531 (2010) [Entomol. Rev. 90 (9), 1127–1152 (2010)].

    Google Scholar 

  111. Saulich, A.Kh. and Musolin, D.L., “Univoltinism and Its Regulation in Some Temperate True Bugs (Heteroptera),” Eur. J. Entomol. 93(3), 507–518 (1996).

    Google Scholar 

  112. 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, Ed. by A.A. Stekolnikov (St. Petersburg State University, St. Petersburg, 2007), pp. 25–106 [in Russian].

    Google Scholar 

  113. Saulich, A.Kh. and Musolin, D.L., “Seasonal Development and Ecology of Anthocorids (Heteroptera, Anthocoridae),” Entomol. Obozr. 88(2), 257–291 (2009) [Entomol. Rev. 89 (5), 501–528 (2009)].

    Google Scholar 

  114. Saulich, A.Kh. and Musolin, D.L., Biology and Ecology of the Predatory Bug Podisus maculiventris (Say) (Heteroptera, Pentatomidae) and Its Possible Use against the Colorado Potato Beetle Leptinotarsa decemlineata Say (Coleoptera, Chrysomelidae): a Teaching Aid (St. Petersburg State Univ., St. Petersburg, 2011a) [in Russian].

    Google Scholar 

  115. 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), 740–774 (2011b) [Entomol. Rev. 92 (1), 1–26 (2012)].

    Google Scholar 

  116. Saulich, A.Kh. and Volkovitsh, T.A., “Univoltinism and Its Regulation in Insects,” Entomol. Obozr. 75(2), 244–258 (1996).

    Google Scholar 

  117. Saulich, A.Kh. and Volkovitsh, T.A., Ecology of Photoperiodism in Insects (St. Petersburg State Univ., St. Petersburg, 2004) [in Russian].

    Google Scholar 

  118. Saunders, D.S., Insect Clocks (Pergamon Press, Oxford, 1976).

    Google Scholar 

  119. Schumacher, F., “Beiträge zur Kenntnis der Biologie der Asopiden,” Z. Wiss. Insectenbiol. 6, 263–266, 376–383, 430–437; 7, 40–47 (1910–1911).

    Google Scholar 

  120. Sharonov, V.V., Tables for Calculation of Natural Illumination and Visibility (USSR Acad. Sci., Moscow, 1945) [in Russian].

    Google Scholar 

  121. Shintani, Y., Masuzawa, Y., Hirose, Y., et al., “Seasonal Occurrence and Diapause Induction of a Predatory Bug Andrallus spinidens (F.) (Heteroptera: Pentatomidae),” Entomol. Sci. 13, 273–279 (2010).

    Google Scholar 

  122. Singh, Z., Southern Green Stink Bug and Its Relationship to Soybeans: Bionomics of the Southern Green Stink Bug Nezara viridula (Hemiptera: Pentatomidae) in Central India (Metropolitan Book Co. Ltd, Delhi, 1973).

    Google Scholar 

  123. Şişli, M.N., “The Effect of the Photoperiod on the Induction and Termination of the Adult Diapause of Aelia rostrata Boh. (Hemiptera: Pentatomidae),” Comm. Fac. Sci. Univ. Ankara 10, 62–69 (1965).

    Google Scholar 

  124. Southwood, T.R.E. and Leston, D., Land and Water Bugs of the British Isles (Frederick Warne and Co., London, 1959).

    Google Scholar 

  125. Sun, X. and Marshall, S.A., “Systematics of Phasia Latreille (Diptera: Tachinidae),” Zootaxa, No. 276, 1–320 (2003).

    Google Scholar 

  126. Takeda, K., Musolin, D.L., and Fujisaki, K., “Dissecting Insect Responses to Climate Warming: Overwintering and Post-Diapause Performance in the Southern Green Stink Bug, Nezara viridula, under Simulated Climate-Change Conditions,” Physiol. Entomol. 35(4), 343–353 (2010).

    Google Scholar 

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

    Google Scholar 

  128. Todd, J.W., “Ecology and Behavior of Nezara viridula,” Annu. Rev. Entomol. 34, 273–292 (1989).

    Google Scholar 

  129. Tomokuni, M., Yasunaga, T., Takai, M., et al., A Field Guide to Japanese Bugs: Terrestrial Heteropterans (Zenkoku Noson Kyoiku Kyokai, Tokyo, 1993) [in Japanese].

    Google Scholar 

  130. Tougou, D., Musolin, D.L., and Fujisaki, K., “Some Like It Hot! Rapid Climate Change Promotes Changes in Distribution Ranges of Nezara viridula and Nezara antennata in Japan,” Entomol. Exp. Appl. 130, 249–258 (2009).

    Google Scholar 

  131. Tyshchenko, V.P., “Physiology of Photoperiodism in Insects,” Trudy Vses. Entomol. Obshch. 59, 1–155 (1977).

    Google Scholar 

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

    Google Scholar 

  133. Tyshchenko, V.P., “Evolution of Seasonal Adaptations in Insects,” Zh. Obshch. Biol. 44(1), 10–22 (1983).

    Google Scholar 

  134. Viktorov, G.A., Ecology of Entomoparasites (Nauka, Moscow, 1976) [in Russian].

    Google Scholar 

  135. Vinokurov, N.N., Kanyukova, E.V., and Golub, V.B., A Catalogue of Heteroptera of the Asian Part of Russia (Nauka, Novosibirsk, 2010) [in Russian].

    Google Scholar 

  136. Volkovitsh, T.A., “Diapause in the Life Cycles of Lacewings (Neuroptera, Chrysopidae),” in Strategies of Adaptations of Terrestrial Arthropods to Adverse Environmental Conditions, Ed. by A.A. Stekolnikov (St. Petersburg State University, St. Petersburg, 2007), pp. 234–304 [in Russian].

    Google Scholar 

  137. Volkovitsh, T.A., Kolesnichenko, L.I., and Saulich, A.Kh., “The Role of Thermorhythms in the Development of the Two-Spotted Stink Bug Perillus bioculatus (Hemiptera, Pentatomidae),” Zool. Zh. 69(6), 70–81 (1990).

    Google Scholar 

  138. Volkovitsh, T.A. and Saulich, A.Kh., “Photoperiodic and Thermal Control of Diapause and Coloration in the Stink Bug Arma custos,” Zool. Zh. 73(10), 26–37 (1994).

    Google Scholar 

  139. Volkovitsh, T.A., Saulich, A.Kh., and Goryshin, N.I., “The Day-Length Sensitive Stage and Accumulation of Photoperiodic Information in the Spined Soldier Bug Podisus maculiventris Say (Heteroptera: Pentatomidae),” Entomol. Obozr. 70(1), 14–22 (1991).

    Google Scholar 

  140. Whitmarsh, R.D., “Life-History Notes on Apateticus cynicus and maculiventris,” J. Econ. Entomol. 9, 51–53 (1916).

    Google Scholar 

  141. Wilde, G.E., “Photoperiodism in Relation to Development and Reproduction in the Green Stink Bug,” J. Econ. Entomol. 62(3), 629–630 (1969).

    Google Scholar 

  142. Yathom, S., “An Outbreak of Dolycoris baccarum L. (Heteroptera: Pentatomidae) on Sunflower in Israel,” Israel J. Entomol. 14, 25–28 (1980).

    Google Scholar 

  143. Yukawa, J., Kiritani, K., Gyoutoku, N., et al., “Distribution Range Shift of Two Allied Species, Nezara viridula and N. antennata (Hemiptera: Pentatomidae), in Japan, Possibly Due to Global Warming,” Appl. Entomol. Zool. 42, 205–215 (2007).

    Google Scholar 

  144. Yukawa, J., Kiritani, K., Kawasawa, T., et al., “Northward Range Expansion by Nezara viridula (Hemiptera: Pentatomidae) in Shikoku and Chugoku Districts, Japan, Possibly Due to Global Warming,” Appl. Entomol. Zool. 44(3), 429–437 (2009).

    Google Scholar 

  145. Zou, D., Wang, M., Zhang, L., et al., “Taxonomic and Bionomic Notes on Arma chinensis (Fallou) (Hemiptera: Pentatomidae: Asopinae),” Zootaxa, No. 3382, 41–52 (2012).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Kh. Saulich.

Additional information

Original Russian Text © A.Kh. Saulich, D.L. Musolin, 2014, published in Entomologicheskoe Obozrenie, 2014, Vol. 93, No. 2, pp. 263–302.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saulich, A.K., Musolin, D.L. Seasonal cycles in stink bugs (Heteroptera, Pentatomidae) from the temperate zone: Diversity and control. Entmol. Rev. 94, 785–814 (2014). https://doi.org/10.1134/S0013873814060013

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0013873814060013

Keywords

Navigation