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Responses of insects to the current climate changes: from physiology and behavior to range shifts

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Abstract

Climate change (first of all the rise in temperature) is currently considered one of the most serious global challenges facing mankind. Here we review the diversity of insect responses to the current climate warming, with particular focus on true bugs (Heteroptera). Insects as ectotherms are bound to respond to the temperature change, and different species respond differently depending on their specific physiological and ecological traits, seasonal cycle, trophic relations, etc. Insect responses to climate warming can be divided into six categories: changes in (1) ranges, (2) abundance, (3) phenology, (4) voltinism, (5) morphology, physiology, and behavior, and (6) relationships with other species and in the structure of communities. Changes in ranges and phenology are easier to notice and record than other responses. Range shifts have been reported more often in Lepidoptera and Odonata than in other insect orders. We briefly outline the history and eco-physiological background of the recent range limit changes in the Southern green stink bug Nezara viridula (Heteroptera, Pentatomidae) in central Japan. Range expansion in individual species can lead to enrichment of local faunas, especially at high latitudes. Phenological changes include not only advances in development in spring but also shifts in phenology later in the season. The phenophases related to the end of activity usually shift to later dates, thus prolonging the period of active development. This may have both positive and negative consequences for the species and populations. As with any other response, the tendencies in phenological changes may vary among species and climatic zones. The proven cases of change in voltinism are rare, but such examples do exist. Application of models based on thermal parameters of development suggests that a rise in temperature by 2°C will result in an increased number of annual generations in many species from different arthropod taxa (up to three or four additional generations in Thysanoptera, Aphidoidea, and Acarina). The warming-mediated changes in physiology, morphology, or behavior are difficult to detect and prove, first of all because of the absence of reliable comparative data. Nevertheless, there are examples of changes in photoperiodic responses of diapause induction and behavioral responses related to search of shelters for summer diapause (aestivation). Since (1) individual species do not exist in isolation and (2) the direction and magnitude of responses even to the same environmental changes vary between species, it may be expected that in many cases the current stable relationships between species will be affected. Thus, unequal range shifts in insects and their host plants may disrupt their trophic interactions near the species’ range boundaries. Studies of responses to climate warming in more than one interrelated species or in entire communities are extremely rare. The loss of synchronism in seasonal development of community members may indicate inability of the higher trophic levels to adapt fully to climate warming or an attempt of the lower trophic level to escape from the pressure of the higher trophic levels. It is generally supposed that many insect species in the Temperate Climate Zone will benefit in some way from the current climate warming. However, there is some experimental evidence of an opposite or at least much more complex response; the influence of warming might be deleterious for some species or populations. It is suggested that species or populations from the cold or temperate climate have sufficient phenotypic plasticity to survive under the conditions of climate warming, whereas species and populations which already suffer from stress under extreme seasonal temperatures in warmer regions may have a limited “maneuver space” since the current temperatures are close to their upper thermal limits. Without genetic changes, even moderate warming will put these species or populations under serious physiological stress. The accumulated data suggest that responses of insects and the entire biota to climate warming will be complex and will vary depending on the rate of warming and ecological peculiarities of species and regions. Physiological responses will vary in their nature, direction, and magnitude even within one species or population, and especially between seasons. The responses will also differ in different seasons. For example, warming may negatively affect nymphal development during the hot season but at the same time accelerate growth and development during the cold season and/or ensure milder and more favorable overwintering conditions for adults. All these factors will affect population dynamics of particular species and relationships among the members of ecosystems. We should keep in mind that (1) not only selected insect species but almost all the species will be affected, (2) temperature is not the only component of the climatic system that is changing, and (3) responses will be different in different seasons. Host plants, phytophagous insects, their competitors, symbionts, predators, parasites, and pathogens will not only respond separately to climate changes; individual responses will further affect the responses of other species, thus making reliable prediction extremely complicated. Responses are expected to (1) be species- or population-specific, (2) concern basically all the aspects of organism/ species biology and ecology (individual physiology, population structure, abundance, local adaptations, phenology, voltinism, and distribution), and (3) occur at scales ranging from an undetectable cellular level to major distribution range shifts or regional extinctions. The scale of insect responses will depend on the extent and rate of climate warming. Slight to moderate warming may cause responses only in a limited number of species with more flexible life cycles, whereas a substantial increase in temperature may affect a greater number of different species and ecological groups.

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References

  1. Adler, L.S., de Valpine, P., Harte, J., and Call, J., “Effects of Long-Term Experimental Warming on Aphid Density in the Field,” J. Kansas Entomol. Soc. 80, 156–168 (2007).

    Article  Google Scholar 

  2. Altermatt, F., “Climatic Warming Increases Voltinism in European Butterflies and Moths,” Proc. Roy. Soc. Ser. B 277(1685), 1281–1287 (2010).

    Article  Google Scholar 

  3. Andrew, N.R. and Hughes, L., “Arthropod Community Structure along a Latitudinal Gradient: Implications for Future Impacts of Climate Change,” Austral. Ecol. 30, 281–297 (2005).

    Article  Google Scholar 

  4. Aono, Y. and Omoto, Y., “Temperature Trends in Kyoto since the Eleventh Century Based on Records of Cherry Blooms,” Nogyo Kisho (Agric. Meteorol.) 49, 263–272 (1994) [in Japanese].

    Google Scholar 

  5. Atkinson, D., “Temperature and Organism Size—a Biological Law for Ectotherms?” Adv. Ecol. Res. 25, 1–58 (1994).

    Article  Google Scholar 

  6. Aukema, B., “Annotated Checklist of Hemiptera-Heteroptera of the Netherlands,” Tijdschr. Entomol. 132, 1–104 (1989).

    Google Scholar 

  7. Aukema, B., “Recent Changes in the Dutch Heteroptera Fauna (Insecta: Hemiptera),” in Changes in Ranges: Invertebrates on the Move. Proc. of the 13th Int. Colloquium of the European Invertebrate Survey. Leiden, 2–5 September 2001, Ed. by M. Reemer, P.J. van Helsdingen, and R.M.J.C. Kleukers (European Invertebrate Survey, Leiden, 2003), pp. 39–52.

    Google Scholar 

  8. Aukema, B., Bos, F., Hermes, D., and Zeinstra, P., “Nieuwe en interessante Nederlandse wantsen II, met een geactualiseerde naamlijst (Hemiptera: Heteroptera),” Nederl. Faun. Med. 23, 37–76 (2005).

    Google Scholar 

  9. Aukema, B. and Hermes, D., “Nieuwe en interessante nederlandse wantsen III (Hemiptera: Heteroptera),” Nederl. Faun. Med. 31, 53–88 (2009).

    Google Scholar 

  10. Babin-Fenske, J., Anand, M., and Alarie, Y., “Rapid Morphological Change in Stream Beetle Museum Specimens Correlates with Climate Change,” Ecol. Entomol. 33, 646–651 (2008).

    Article  Google Scholar 

  11. Bale, J.S., Harrington, R., and Howling, G.G., “Aphids and Winter Weather I. Aphids and Climate Change,” in Proc. 4th European Congr. of Entomology, Budapest, Vol. 1 (Hungarian Natural History Museum, Budapest, 1992), pp. 139–143.

    Google Scholar 

  12. Bale, J.S. and Hayward, S.A.L., “Insect Overwintering in a Changing Climate,” J. Exp. Biol. 213, 980–994 (2010).

    Article  PubMed  CAS  Google Scholar 

  13. Bale, J.S., Masters, G.J., Hodkinson, I.D., et al., “Herbivory in Global Climate Change Research: Direct Effects of Rising Temperature on Insect Herbivores,” Glob. Change Biol. 8, 1–16 (2002).

    Article  Google Scholar 

  14. Barclay, M.V.L., “The Green Vegetable Bug Nezara viridula (L., 1758) (Hem.: Pentatomidae) New to Britain,” Entomol. Record J. Variation 116, 55–58 (2004).

    Google Scholar 

  15. Barclay, M.V.L. and Nau, B.S., “A Second Species of Tamarisk Bug in Britain, Tuponia brevirostris Reuter, and the Current Status of T. mixticolor (A. Costa) (Hem., Miridae),” Entomol. Month. Mag. 139, 176–177 (2003).

    Google Scholar 

  16. Böhm, R., Auer, I., Brunetti, M., et al., “Regional Temperature Variability in the European Alps: 1760–1998 from Homogenized Instrumental Time Series,” Int. J. Climatol. 21, 1779–1801 (2001).

    Article  Google Scholar 

  17. Both, C., van Asch, M., Bijlsma, R.G., et al., “Climate Change and Unequal Phenological Changes across Four Trophic Levels: Constraints or Adaptations?” J. Animal Ecol. 78, 73–83 (2009).

    Article  Google Scholar 

  18. Bradshaw, W.E. and Holzapfel, C.M., “Genetic Shift in Photoperiodic Response Correlated with Global Warming,” Proc. Nat. Acad. Sci. USA 98, 14509–14511 (2001).

    Article  PubMed  CAS  Google Scholar 

  19. Bradshaw, W.E. and Holzapfel, C.M., “Genetic Response to Rapid Climate Change: It’s Seasonal Timing that Matters,” Molec. Ecol. 17, 157–166 (2008).

    Article  CAS  Google Scholar 

  20. Burton, J.F., “The Apparent Effects of Climate Changes since 1850 on European Lepidoptera,” Mem. Soc. R. Entomol. Belg. 38, 125–144 (1998).

    Google Scholar 

  21. Chamaillé-Jammes, S., Massot, M., Aragon, P., and Clobert, J., “Global Warming and Positive Fitness Response in Mountain Populations of Common Lizards Lacerta vivipara,” Glob. Change Biol. 12, 392–402 (2006).

    Article  Google Scholar 

  22. 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, 237–247 (2007).

    Article  Google Scholar 

  23. Crozier, L., “Warmer Winters Drive Butterfly Range Expansion by Increasing Survivorship,” Ecology 85, 231–241 (2004).

    Article  Google Scholar 

  24. Dahlhoff, E.P., Fearnley, S.L., Bruce, D.A., et al., “Effects of Temperature on Physiology and Reproductive Success of a Montane Leaf Beetle: Implications for Persistence of Native Populations Enduring Climate Change,” Phys. Biochem. Zool. 81, 718–732 (2008).

    Article  Google Scholar 

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

    Google Scholar 

  26. Davis, A.J., Jenkinson, L.S., Lawton, J.H., et al., “Making Mistakes when Predicting Shifts in Species Range in Response to Global Warming,” Nature 391, 783–786 (1998a).

    Article  PubMed  CAS  Google Scholar 

  27. Davis, A.J., Lawton, J.H., Shorrocks, B., and Jenkinson, L.S., “Individualistic Species Responses Invalidate Simple Physiological Models of Community Dynamics under Global Environmental Change,” J. Animal Ecol. 67, 600–612 (1998b).

    Article  Google Scholar 

  28. Deutsch, C.A., Tewksbury, J.J., Huey, R.B., et al., “Impacts of Climate Warming on Terrestrial Ectotherms across Latitude,” Proc. Natl Acad. Sci. USA 105, 6668–6672 (2008).

    Article  PubMed  CAS  Google Scholar 

  29. Dingemanse, N.J. and Kalkman, V.J., “Changing Temperature Regimes have Advanced the Phenology of Odonata in the Netherlands,” Ecol. Entomol. 33, 394–402 (2008).

    Article  Google Scholar 

  30. Entwistle, J.C. and Dixon, A.F.G., “The Effect of Augmenting Grain Aphid (Sitobion avenae) Numbers in a Field of Winter Wheat in Spring on the Aphid’s Abundance in Summer and Its Relevance to the Forecasting of Outbreaks,” Annals Appl. Biol. 114, 397–408 (1989).

    Article  Google Scholar 

  31. Estrella, N., Sparks, T.H., and Menzel, A., “Trends and Temperature Response in the Phenology of Crops in Germany,” Glob. Change Biol. 13, 1737–1747 (2007).

    Article  Google Scholar 

  32. Feeley, K.J., Wright, S.J., Nur Supardi, M.N., et al., “Decelerating Growth in Tropical Forest Trees,” Ecol. Letters 10, 461–469 (2007).

    Article  Google Scholar 

  33. 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).

  34. Flanagan, J. and Coldwell, J., “Stictopleurus punctatonervosus (Hemiptera: Rhopalidae) New to Yorkshire and a Summary Review of Other Rhopalidae in Yorkshire,” Sorby Record (UK), No. 44, 33–37 (2008).

  35. Forister, M.L. and Shapiro, A.M., “Climatic Trends and Advancing Spring Flight of Butterflies in Lowland California,” Glob. Change Biol. 9, 1130–1135 (2003).

    Article  Google Scholar 

  36. GISS (Goddard Institute of Space Studies), 2009: Second Warmest Year on Record; End of Warmest Decade (2010), http://www.nasa.gov/topics/earth/features/tempanalysis-2009.html.

  37. Gomi, T., Nagasaka, M., Fukuda, T., and Hagihara, H., “Shifting of the Life Cycle and Life-History Traits of the Fall Webworm in Relation to Climate Change,” Entomol. Exp. Appl. 125, 179–184 (2007).

    Article  Google Scholar 

  38. Gomi, T. and Takeda, M., “Changes in Life-History Traits in the Fall Webworm within Half a Century after Introduction to Japan,” Functional Ecol. 10, 384–389 (1996).

    Article  Google Scholar 

  39. Guo, K., Hao, S.-G., Sun, J.S., and Kang, L., “Differential Responses to Warming and Increased Precipitation among Three Contrasting Grasshopper Species,” Glob. Change Biol. 15, 2539–2548 (2009).

    Article  Google Scholar 

  40. Harada, T., Nitta, S., and Ito, K., “Photoperiodic Changes According to Global Warming in Wing-Form Determination and Diapause Induction of a Water Strider, Aquarius paludum (Heteroptera: Gerridae),” Appl. Entomol. Zool. 40, 461–466 (2005).

    Article  Google Scholar 

  41. Harada, T. and Numata, H., “Two Critical Day Lengths for the Determination of Wing Forms and the Induction of Adult Diapause in the Water Strider, Aquarius paludum,” Naturwissenschaften 80, 430–432 (1993).

    Article  Google Scholar 

  42. Harrington, R., Bale, J.S., and Tatchell, G.M., “Aphids in a Changing Climate,” in Insects in a Changing Environment, Ed. by R. Harrington and N.E. Stork (Acad. Press, London, 1995), pp. 125–155.

    Google Scholar 

  43. Harrington, R., Clark, S.J., Welham, S.J., et al., “European Union EXAMINE Consortium. Environmental Change and the Phenology of European Aphids,” Glob. Change Biol. 13, 1550–1564 (2007).

    Article  Google Scholar 

  44. Harrington, R., Fleming, R.A., and Woiwod, I.P., “Climate Change Impacts on Insect Management and Conservation in Temperate Regions: Can They be Predicted?” Agric. Forest Entomol. 3, 233–240 (2001).

    Article  Google Scholar 

  45. Harrington, R. and Stork, N.E. (Eds.), Insects in a Changing Environment (Acad. Press, London, 1995).

    Google Scholar 

  46. Harrington, R., Tatchell, G.M., and Bale, J.S., “Weather, Life Cycle Strategy and Spring Populations of Aphids,” Acta Phytopathol. Entomol. Hungarica 25, 423–432 (1990).

    Google Scholar 

  47. Hassall, C., Thompson, D.J., French, G.C., and Harvey, I.F., “Historical Changes in the Phenology of British Odonata are Related to Climate,” Glob. Change Biol. 13, 933–941 (2007).

    Article  Google Scholar 

  48. Helmuth, B., Broitman, B.R., Yamane, L., et al., “Organismal Climatology: Analyzing Environmental Variability at Scales Relevant to Physiological Stress,” J. Exp. Biol. 213, 995–1003 (2010).

    Article  PubMed  Google Scholar 

  49. Helmuth, B., Kingsolver, J.G., and Carrington, E., “Biophysics, Physiological Ecology, and Climate Change: Does Mechanism Matter?” Ann. Rev. Physiol. 67, 177–201 (2005).

    Article  CAS  Google Scholar 

  50. Hickling, R., Roy, D.B., Hill, J.K., et al., “The Distributions of a Wide Range of Taxonomic Groups are Expanding Polewards,” Glob. Change Biol. 12, 450–455 (2006).

    Article  Google Scholar 

  51. Hickling, R., Roy, D.B., Hill, J.K., and Thomas, C.D., “A Northward Shift of Range Margins in British Odonata,” Glob. Change Biol. 11, 502–506 (2005).

    Article  Google Scholar 

  52. Hill, J.K., Thomas, C.D., Fox, R., et al., “Responses of Butterflies to Twentieth Century Climate Warming: Implications for Future Ranges,” Proc. Roy. Soc. Ser. B 269, 2163–2171 (2002).

    Article  CAS  Google Scholar 

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

    Google Scholar 

  54. Houghton, J., Global Warming. The Complete Briefing. 3rd Ed. (Cambridge Univ. Press, Cambridge, 2004).

    Book  Google Scholar 

  55. Høye, T.T., Hammel, J.U., Fuchs, T., and Toft, S., “Climate Change and Sexual Size Dimorphism in an Arctic Spider,” Biol. Lett. 5, 542–544 (2009).

    Article  PubMed  Google Scholar 

  56. Hulme, M., Jenkins, G.L., Lu, X., et al., Climate Change Scenarios for the United Kingdom: The UKCIP02 Scientific Report (Tyndall Centre for Climate Change Research, School of Environmental Sciences, University of East Anglia, Norwich, 2002).

    Google Scholar 

  57. IPCC (Intergovernmental Panel on Climate Change). Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (IPCC, Geneva, Switzerland, 2007a).

  58. IPCC (Intergovernmental Panel on Climate Change). Climate Change 2007: The Physical Science Basis. Summary for Policymakers. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (IPCC, Geneva, Switzerland, 2007b).

  59. Jepsen, J.U., Hagen, S.B., Ims, R.A., and Yoccoz, N.G., “Climate Change and Outbreaks of the Geometrids Operophtera brumata and Epirrita autumnata in Subarctic Birch Forest: Evidence of a Recent Outbreak Range Expansion,” J. Animal Ecol. 77, 257–264 (2008).

    Article  Google Scholar 

  60. Jones, R.A., “Brachycarenus tigrinus (Schilling) (Hemiptera: Rhopalidae) New to Britain,” British J. Entomol. Nat. Hist. 17, 137–141 (2004).

    Google Scholar 

  61. Jones, W.A., “World Review of the Parasitoids of the Southern Green Stink Bug Nezara viridula (L.) (Heteroptera: Pentatomidae),” Ann. Entomol. Soc. Amer. 81, 262–273 (1988).

    Google Scholar 

  62. Jönsson, A.M., Appelberg, G., Harding, S., and Bärring, L., “Spatio-Temporal Impact of Climate Change on the Activity and Voltinism of the Spruce Bark Beetle, Ips typographus,” Glob. Change Biol. 15, 486–499 (2009).

    Article  Google Scholar 

  63. Jönsson, A.M., Harding, S., Bärring, L., and Ravn, H.P., “Impact of Climate Change on the Population Dynamics of Ips typographus in Southern Sweden,” Agric. Forest Meteorol. 146, 70–81 (2007).

    Article  Google Scholar 

  64. Jump, A.S., Hunt, J.M., and Peñuelas, J., “Rapid Climate Change-Related Growth Decline at the Southern Range Edge of Fagus sylvatica,” Glob. Change Biol. 12, 2163–2174 (2006).

    Article  Google Scholar 

  65. 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,” Jap. J. Appl. Entomol. Zool. 15, 191–196 (1961).

    Article  Google Scholar 

  66. Kato, H., “Statistical Method for Separating Urban Effect Trends from Observed Temperature Data and Its Application to Japanese Temperature Records,” J. Meteorol. Soc. Jap. 74, 639–653 (1996).

    Google Scholar 

  67. 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, 117–128 (2006).

    Article  PubMed  CAS  Google Scholar 

  68. Kirby, P., Stewart, A.J.A., and Wilson, M.R., “True Bugs, Leaf- and Planthoppers, and Their Allies,” in The Changing Wildlife of Great Britain and Ireland, Ed. by D.L. Hawksworth (Taylor, Francis, London, 2001), pp. 262–299.

    Google Scholar 

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

    Google Scholar 

  70. Kiritani, K., “Predicting Impact of Global Warming on Population Dynamics and Distribution of Arthropods in Japan,” Popul. Ecol. 48, 5–12 (2006).

    Article  Google Scholar 

  71. Kiritani, K., “The Impact of Global Warming and Land-Use Change on the Pest Status of Rice and Fruit Bugs (Heteroptera) in Japan,” Glob. Change Biol. 13, 1586–1595 (2007).

    Article  Google Scholar 

  72. Kiritani, K., “Impacts of Global Warming on Nezara viridula and Its Native Congeneric Species,” J. Asia-Pacific Entomol. 14, 221–226 (2011).

    Article  Google Scholar 

  73. 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),” Jap. J. Appl. Entomol. Zool. 6, 242–246 (1962).

    Article  Google Scholar 

  74. Kiritani, K., Hokyo, N., and Kimura, K., “Factors Affecting the Winter Mortality in the Southern Green Stink Bug, Nezara viridula L.,” Ann. Soc. Entomol. France. Nouv. Sér. 2(Sunn Pest Memoirs 9), 199–207 (1966).

    Google Scholar 

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

    Article  Google Scholar 

  76. Klapwijk, M.J., Gröbler, B.C., Ward, K., et al., “Influence of Experimental Warming and Shading on Host-Parasitoid Synchrony,” Glob. Change Biol. 16, 102–112 (2010).

    Article  Google Scholar 

  77. Lange, H., Økland, B., and Krokene, P., “To Be or Twice to Be? The Life Cycle Development of the Spruce Bark Beetle under Climate Change,” in Unifying Themes in Complex Systems. Part 2, Ed. by A.A. Minai, D. Braha, and Y. Bar-Yam (Springer Verlag, Berlin, 2010), pp. 251–258.

    Chapter  Google Scholar 

  78. Leather, S.R., Walters, K.F.A., and Bale, J.S., The Ecology of Insect Overwintering (Cambridge Univ. Press, Cambridge, 1993).

    Book  Google Scholar 

  79. Linderholma, H.W., “Growing Season Changes in the Last Century,” Agric. Forest Meteorol. 137, 1–14 (2006).

    Article  Google Scholar 

  80. Logan, J.A., Régnière, J., and Powell, J., “Assessing the Impacts of Global Warming on Forest Pest Dynamics,” Frontiers Ecol. Environ. 1, 130–137 (2003).

    Article  Google Scholar 

  81. Maistrello, L., Lombroso, L., Pedroni, E., et al., “Summer Raids of Arocatus melanocephalus (Heteroptera, Lygaeidae) in Urban Buildings in Northern Italy: Is Climate Change to Blame?” J. Thermal Biol. 31, 594–598 (2006).

    Article  Google Scholar 

  82. Malcolm, J.R., Liu, C., Nelson, R.P., et al., “Global Warming and Extinctions of Endemic Species from Biodiversity Hotspots,” Conserv. Biol. 20, 538–548 (2006).

    Article  PubMed  Google Scholar 

  83. Martín-Vertedor, D., Ferrero-García, J.J., and Torres-Vila, L.M., “Global Warming Affects Phenology and Voltinism of Lobesia botrana in Spain,” Agric. Forest Entomol. 12, 169–176 (2010).

    Article  Google Scholar 

  84. Masters, G.J., Brown, V.K., Clarke, I.P., et al., “Direct and Indirect Effects of Climate Change on Insect Herbivores: Auchenorrhyncha (Homoptera),” Ecol. Entomol. 23, 45–52 (1998).

    Article  Google Scholar 

  85. Meiri, S., Guy, D., Dayan, T., and Simberloff, D., “Global Change and Carnivore Body Size: Data are Stasis,” Glob. Ecol. Biogeogr. 18, 240–247 (2009).

    Article  Google Scholar 

  86. Menzel, A., “Trends in Phenological Phases in Europe between 1951 and 1996,” Int. J. Biometeorol. 44, 76–81 (2000).

    Article  PubMed  CAS  Google Scholar 

  87. Menzel, A. and Dose, V., “Analysis of Long-Term Time Series of the Beginning of Flowering by Bayesian Function Estimation,” Meteorol. Zeitschrift 14, 429–434 (2005).

    Article  Google Scholar 

  88. Menzel, A., Sparks, T.H., Estrella, N., et al., “European Phenological Response to Climate Change Matches the Warming Pattern,” Glob. Change Biol. 12, 1969–1976 (2006).

    Article  Google Scholar 

  89. Mikkola, K., “Population Trends of Finnish Lepidoptera during 1961-1996,” Entomol. Fenn. 3, 121–143 (1997).

    Google Scholar 

  90. Miles, J.E., Bale, J.S., and Hodkinson, I.D., “Effects of Temperature Elevation on the Population Dynamics of the Upland Heather Psyllid Strophingia ericae (Curtis) (Homoptera: Psylloidea),” Glob. Change Biol. 3, 291–297 (2003).

    Article  Google Scholar 

  91. Moise, E.R.D. and Henry, H.A.L., “Like Moths to a Street Lamp: Exaggerated Animal Densities in Plot-Level Global Change Field Experiments,” Oikos 119, 791–795 (2010).

    Article  Google Scholar 

  92. Møller, A.P., Rubolini, D., and Lehikoinen, E., “Populations of Migratory Bird Species that did not Show a Phenological Response to Climate Change are Declining,” Proc. Natl Acad. Sci. USA 105, 16195–16200 (2008).

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  94. Musolin, D.L. and Fujisaki, K., “Changes in Ranges: Trends in Distribution of True Bugs (Heteroptera) under Conditions of the Current Climate Warming,” Russ. Entomol. J. 15, 175–179 (2006).

    Google Scholar 

  95. 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, 65–74 (2003a).

    Article  Google Scholar 

  96. 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, 694–703 (2003b).

    Article  Google Scholar 

  97. 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),” Glob. Change Biol. 16, 73–87 (2010).

    Article  Google Scholar 

  98. 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. Control 31, 91–98 (2004).

    Article  Google Scholar 

  99. Nakata, M., “Control of the Fall Webworm, Hyphantria cunea Drury, in Japan,” Shokubutsuboueki Shiryokan Shiryo 9, 1–93 (1996) [in Japanese].

    Google Scholar 

  100. Nau, B.S., “Range-Changes in Some Species of Hemiptera-Heteroptera in Bedfordshire,” Entomol. Mon. Mag. 133, 261–262 (1997).

    Google Scholar 

  101. Nau, B.S. and Brooke, S.E., “The Contrasting Range Expansion of Two Species of Deraeocoris (Hemiptera-Heteroptera: Miridae) in South-East England,” British J. Entomol. Nat. Hist. 16, 44–45 (2003).

    Google Scholar 

  102. Newman, J.A., “Climate Change and the Fate of Cereal Aphids in Southern Britain,” Glob. Change Biol. 11, 940–944 (2005).

    Article  Google Scholar 

  103. Nonaka, K. and Nagai, K., “Studies on the Biology of Pentatomids and Their Control. 6. Developmental Rate of the Southern Green Stink Bug,” Proc. Assoc. Plant Protection Kyushu 24, 80–81 (1978) [in Japanese].

    Article  Google Scholar 

  104. Ohira, Y., “Outbreak of the Stink Bugs Attacking Fruit Trees in 2002,” Shokubutsu Boeki [Plant Protection] 57, 164–168 (2003) [in Japanese].

    Google Scholar 

  105. Oho, N. and Kiritani, K., “Bionomics and Control of the Southern Green Stink Bug,” Shokubutsu Boeki [Plant Protection] 14, 237–241 (1960) [in Japanese].

    Google Scholar 

  106. 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 

  107. Parmesan, C., “Detection of Range Shifts: General Methodological Issues and Case Studies Using Butterflies,” in “Fingerprints” of Climate Change: Adapted Behavior and Shifting Species Ranges, Ed. by G.-R. Walter, C.A. Burga, and P.J. Edwards (Kluwer Acad. / Plenum Publ., New York, 2001), pp. 57–76.

    Google Scholar 

  108. Parmesan, C., “Ecological and Evolutionary Responses to Recent Climate Change,” Ann. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).

    Article  Google Scholar 

  109. Parmesan, C., “Influences of Species, Latitudes and Methodologies on Estimates of Phenological Response to Global Warming,” Glob. Change Biol. 13, 1860–1872 (2007).

    Article  Google Scholar 

  110. Parmesan, C., Ryrholm, N., Stefanescu, C., et al., “Poleward Shifts in Geographical Ranges of Butterfly Species Associated with Regional Warming,” Nature 399, 579–583 (1999).

    Article  CAS  Google Scholar 

  111. Parmesan, C. and Yohe, G., “A Globally Coherent Fingerprint of Climate Change Impacts across Natural Systems,” Nature 421, 37–42 (2003).

    Article  PubMed  CAS  Google Scholar 

  112. Parry, M.L., “The Potential Impact on Agriculture of the ‘Greenhouse Effect’,” in The “Greenhouse Effect” and UK Agriculture, Ed. by R.M. Bennett (Centre for Agricultural Strategy, Reading, 1989), pp. 27–46.

    Google Scholar 

  113. Peng, S., Huang, J., Sheehy, J.E., et al., “Rice Yields Decline with Higher Night Temperature from Global Warming,” Proc. Natl Acad. Sci. USA 101, 9971–9975 (2004).

    Article  PubMed  CAS  Google Scholar 

  114. Pollard, E., Moss, D., and Yates, T.J., “Population Trends of Common British Butterflies at Monitored Sites,” J. Appl. Ecol. 32, 9–16 (1995).

    Article  Google Scholar 

  115. Pöyry, J., Luoto, M., Heikkinen, R.K., et al., “Species Traits Explain Recent Range Shifts of Finnish Butterflies,” Glob. Change Biol. 15, 732–743 (2009).

    Article  Google Scholar 

  116. Rabitsch, W., “Alien True Bugs of Europe (Insecta: Hemiptera: Heteroptera),” Zootaxa, No. 1827, 1–44 (2008a).

  117. Rabitsch, W., “The Times They are A-Changin’: Driving Forces of Recent Additions to the Heteroptera Fauna of Austria,” in Advances in Heteroptera Research (Festschrift in Honor of 80th Anniversary of Michail Josifov), Ed. by S. Grozeva and N. Simov (Pensoft Publ., Sofia, 2008b), pp. 309–326.

    Google Scholar 

  118. Rahmstorf, S. and Schellnhuber, H.J., Der Klimawandel: Diagnose, Prognose, Therapie (Verlag C.H. Beck, München, 2007; OGI, Moscow, 2009) [in Russian].

    Google Scholar 

  119. Reemer, M., van Helsdingen, P.J., and Kleukers, R.M.J.C. (Eds.), Changes in Ranges: Invertebrates on the Move. Proc. 13th Int. Colloquium of the European Invertebrate Survey. Leiden, 2–5 September 2001 (European Invertebrate Survey, Leiden, 2003).

    Google Scholar 

  120. 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 Entomological Society, Wageningen, 2006), pp. 233–414.

    Google Scholar 

  121. Root, T.L., Price, J.T., Hall, K.R., et al., “Fingerprints of Global Warming on Wild Animals and Plants,” Nature 421, 57–60 (2003).

    Article  PubMed  CAS  Google Scholar 

  122. Rosenzweig, C., Karoly, D., Vicarelli, M., et al., “Attributing Physical and Biological Impacts to Anthropogenic Climate Change,” Nature 453, 353–357 (2008).

    Article  PubMed  CAS  Google Scholar 

  123. Roth, S. and Masters, G., Effects of Climate Change on the Heteropteran Community in Calcareous Grasslands. British Ecological Society Grant Report Database (2000), http://www.britishecologicalsociety.org/grants/reports/archives.php.

  124. Roy, D.B., Rothery, P., Moss, D., et al., “Butterfly Numbers and Weather: Predicting Historical Trends in Abundance and the Future Effects of Climate Change,” J. Animal Ecol. 70, 201–217 (2001).

    Article  Google Scholar 

  125. Roy, D.B. and Sparks, T.H., “Phenology of British Butterflies and Climate Change,” Glob. Change Biol. 6, 407–416 (2000).

    Article  Google Scholar 

  126. Sameshima, T., “Infestation and Damage Caused by the Southern Green Stink Bug,” Shokubutsu Boeki [Plant Protection] 14, 242–246 (1960) [in Japanese].

    Google Scholar 

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

    Google Scholar 

  128. Schwartz, M.W., Iverson, L.R., Prasad, A.M., et al., “Predicting Extinctions as a Result of Climate Change,” Ecology 87, 1611–1615 (2006).

    Article  PubMed  Google Scholar 

  129. Schweiger, O., Settele, J., Kudrna, O., et al., “Climate Change can Cause Spatial Mismatch of Trophically Interacting Species,” Ecology 89, 3472–3479 (2008).

    Article  PubMed  Google Scholar 

  130. Scudder, G.G.E. and Foottit, R.G., “Alien True Bugs (Hemiptera: Heteroptera) in Canada: Composition and Adaptations,” Can. Entomol. 138, 24–51 (2006).

    Article  Google Scholar 

  131. Shardlow, M.E.A. and Taylor, R., “Is the Southern Green Shield Bug, Nezara viridula (L.) (Hemiptera: Pentatomidae) Another Species Colonizing Britain due to Climate Change?” Brit. J. Entomol. Nat. Hist. 17, 143–146 (2004).

    Google Scholar 

  132. Sherry, R.A., Zhou, X., Gu, S., et al., “Divergence of Reproductive Phenology under Climate Warming,” Proc. Natl. Acad. Sci. USA 104, 198–202 (2007).

    Article  PubMed  CAS  Google Scholar 

  133. Shoo, L.P., Williams, S.E., and Hero, J.M., “Detecting Climate Change Induced Range Shifts: Where and How Should We be Looking?” Austr. Ecol. 31, 22–29 (2006).

    Article  Google Scholar 

  134. Skirvin, D., Perry, J., and Harrington, R., “The Effect of Climate Change on an Aphid-Coccinellid Interaction,” Glob. Change Biol. 3, 1–11 (1997).

    Article  Google Scholar 

  135. Smith, R.M., Baker, R.H.A., Malumphy, C.P., et al., “Recent Non-Native Invertebrate Plant Pest Establishments in Great Britain: Origins, Pathways, and Trends,” Agric. Forest Entomol. 9, 307–326 (2007).

    Article  Google Scholar 

  136. Sokolov, L.V., Climate in the Life of Plants and Animals (Tessa, St. Petersburg, 2010) [in Russian].

    Google Scholar 

  137. Southwood, T.R.E., Henderson, P.A., and Woiwod, I.P., “Stability and Changes over 67 Years—the Community of Heteroptera as Caught in a Light-Trap at Rothamsted, UK,” Eur. J. Entomol. 100, 557–561 (2003).

    Google Scholar 

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

    Google Scholar 

  139. Sparks, T.H., Huber, K., and Dennis, R.L.H., “Complex Phenological Responses to Climate Warming Trends? Lessons from History,” Eur. J. Entomol. 103, 379–386 (2006).

    Google Scholar 

  140. Sparks, T.H. and Menzel, A., “Observed Changes in Seasons: an Overview,” Intern. J. Climatol. 22, 1715–1725 (2002).

    Article  Google Scholar 

  141. Stefanescu, C., Penuelas, J., and Filella, I., “Effects of Climatic Change on the Phenology of Butterflies in the Northwest Mediterranean Basin,” Glob. Change Biol. 9, 1494–1506 (2003).

    Article  Google Scholar 

  142. Strathdee, A.T., Bale, J.S., Block, W.C., et al., “Effects of Temperature Elevation on a Field Population of Acyrthosiphon svalbardicum (Hemiptera: Aphididae) on Spitsbergen,” Oecologia 96, 457–465 (1993).

    Article  Google Scholar 

  143. 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, 343–353 (2010).

    Article  Google Scholar 

  144. Teplitsky, C., Mills, J.A., Alho, J.S., et al., “Bergmann’s Rule and Climate Change Revisited: Disentangling Environmental and Genetic Responses in a Wild Bird Population,” Proc. Natl Acad. Sci. USA 105, 13492–13496 (2008).

    Article  PubMed  CAS  Google Scholar 

  145. Thomas, C.D., “Climate, Climate Change and Range Boundaries,” Diversity and Distributions 16, 488–495 (2010).

    Article  Google Scholar 

  146. Thomas, C.D., Franco, A.M.A., and Hill, J.K., “Range Retractions and Extinction in the Face of Climate Warming,” Trends Ecol. Evol. 21, 415–416 (2006).

    Article  PubMed  Google Scholar 

  147. Tixier, G., Wilson, K.P., and Williams, D.D., “Exploration of the Influence of Global Warming on the Chironomid Community in a Manipulated Shallow Groundwater System,” Hydrobiol. 624, 13–27 (2009).

    Article  Google Scholar 

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

    Article  Google Scholar 

  149. 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 

  150. 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).

    Article  Google Scholar 

  151. Tryjanowski, P., Sparks, T., Rybacki, M., and Berger, L., “Is Body Size of the Water Frog Rana esculenta Complex Responding to Climate Change?” Naturwissenschaften 93, 110–113 (2006).

    Article  PubMed  CAS  Google Scholar 

  152. Utkina, I.A. and Rubtsov, V.V., “The Modern Views on the Effects of Climatic Changes on Forest Phyllophages,” in Production and Structure of Forest Biogeocenoses. Theory and Experiment (in the Memory of A.I. Utkin), Ed. by M.G. Romanovskii (Institute of Forestry RAS and KMK Sci. Press, Moscow, 2009), pp. 286–312 [in Russian].

    Google Scholar 

  153. Van Asch, M. and Visser, M.E., “Phenology of Forest Caterpillars and Their Host Trees: The Importance of Synchrony,” Ann. Rev. Entomol. 52, 37–55 (2007).

    Article  CAS  Google Scholar 

  154. Verbeek, K. (Ed.), De Toestand van het Klimaat in Nederland 2003 (Koninklijk Nederlands Meteorologisch Instituut, De Bilt, 2003).

    Google Scholar 

  155. Villalpando, S.N., Williams, R.S., and Norby, R.J., “Elevated Air Temperature Alters an Old-Field Insect Community in a Multifactor Climate Change Experiment,” Glob. Change Biol. 15, 930–942 (2009).

    Article  Google Scholar 

  156. Visser, M.E. and Both, C., “Shifts in Phenology due to Global Climate Change: The Need for a Yardstick,” Proc. Roy. Soc. Ser. B 272(1581), 2561–2569 (2005).

    Article  Google Scholar 

  157. Visser, M.E., Holleman, L.J.M., and Gienapp, P., “Shifts in Caterpillar Biomass Phenology due to Climate Change and Its Impact on the Breeding Biology of an Insectivorous Bird,” Oecologia 147, 164–172 (2006).

    Article  PubMed  Google Scholar 

  158. Walther, G.-R., Post, E., Convey, P., et al., “Ecological Responses to Recent Climate Change,” Nature 416, 389–395 (2002).

    Article  PubMed  CAS  Google Scholar 

  159. Walther, G.-R., Roques, A., Hulme, P.E., et al., “Alien Species in a Warmer World: Risks and Opportunities,” Trends Ecol. Evol. 24, 686–693 (2009).

    Article  PubMed  Google Scholar 

  160. Ward, N.L. and Masters, G.J., “Linking Climate Change and Species Invasion: An Illustration Using Insect Herbivores,” Glob. Change Biol. 13, 1605–1615 (2007).

    Article  Google Scholar 

  161. Warren, M.S., “The Conservation of British Butterflies,” in The Ecology of Butterflies in Britain, Ed. by R.L.H. Dennis (Oxford Univ. Press, Oxford, 1992), pp. 246–274.

    Google Scholar 

  162. Whittaker, J.B. and Tribe, N.P., “Predicting Numbers of an Insect (Neophilaenus lineatus: Homoptera) in a Changing Climate,” J. Anim. Ecol. 67, 987–991 (1998).

    Article  Google Scholar 

  163. Woiwod, I.P. and Harrington, R., “Flying in the Face of Change,” in The Rothamsted Insect Survey. Long Term Research in Agricultural and Ecological Sciences, Ed. by R.A. Leigh and A.E. Johnson (CABI, Wallingford, 1994), pp. 321–342.

    Google Scholar 

  164. Yamamura, K. and Kiritani, K., “A Simple Method to Estimate the Potential Increase in the Number of Generations under Global Warming in Temperate Zone,” Appl. Entomol. Zool. 33, 289–298 (1998).

    Google Scholar 

  165. Yom-Tov, Y., Yom-Tov, S., Wright, J., et al., “Recent Changes in Body Weight and Wing Length among Some British Passerine Birds,” Oikos 112, 91–101 (2006).

    Article  Google Scholar 

  166. Yukawa, J. and Kiritani, K., “Polymorphism in the Southern Green Stink Bug,” Pacific Insects 7, 639–642 (1965).

    Google Scholar 

  167. 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).

    Article  Google Scholar 

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Original Russian Text © D.L. Musolin, A.Kh. Saulich, 2012, published in Entomologicheskoe Obozrenie, 2012, Vol. 91, No. 1, pp. 3–35.

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Musolin, D.L., Saulich, A.K. Responses of insects to the current climate changes: from physiology and behavior to range shifts. Entmol. Rev. 92, 715–740 (2012). https://doi.org/10.1134/S0013873812070019

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